Antiandrogenic and estrogenic characteristics of oleic acid: Experimental design incorporating endocrinal, testicular, and sperm analysis
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Abstract
This research was to investigate whether in utero exposure to oleic acid (OA) could modify the antiandrogenic and estrogenic endocrine functions of the testis during puberty. Pregnant rats were grouped into four groups, with five rats in each group, as follows: control was given 1 mL/kg of olive oil; pretreatment was given 1000 mg/kg OA for seven days before mating; D7 was given 1000 mg/kg OA at gestation day (GD)1–7; and D14 was given 1000 mg/kg of OA at GD8–14. The male offspring delivered were studied into puberty. Hormone levels, age of puberty, and oxidative parameters were determined. The estrogenic properties of oleic acid observed in this study included decreased serum testosterone and a reduction in the epididymis, prostate, and testis weights. Decreased sperm motility and viability, decreased testosterone synthesis, reduced weight of androgen-dependent organs, and delayed onset of puberty were reported as anti-androgenic properties. Testicular MDA levels were significantly higher in OA-exposed rats, compared to control rats. In conclusion, although OA possesses both estrogenic and antiandrogenic properties, the estrogenic characteristics were less pronounced. The antiandrogenic characteristics, steroid hormone inhibition, decrease in sperm variables, and increase in oxidative stress were more distinct.
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Adekunbi, D. A., Ogunsola, O. A., Oyelowo, O. T., Aluko, E. O., Popoola, A. A., and Akinboboye, O. O. (2016). Consumption of high sucrose and/or high salt diet alters sperm function in male Sprague-Dawley rats. Egyptian Journal of Basic and Applied Sciences, 3(2), 194–201.
Aisoni, J. B., Oyelowo, O. T., and Morenikeji, O. A. (2022). Evaluation of pituitary-testicular axis and lipid profile levels in male Wistar rats administered extra virgin olive oil versus oleic acid with a normal diet. Journal of Basic and Social Pharmacy Research, 2(5), 30–39.
Akamine, K., Koyama, T., and Yazawa, K. (2009). Banana peel extract suppressed prostate gland enlargement in testosterone-treated mice. Bioscience Biotechnology Biochemistry, 73(9), 1911–1914.
Aly, H. A. A., and Azhar, A. S. (2013). Methoxychlor-induced biochemical alterations and disruption of spermatogenesis in adult rats. Reproductive Toxicology, 40, 8–15.
Aly, H. A., Hassan, M. H., El-Beshbishy, H. A., Alahdal, A. M., and Osman, A.-M. M. (2016). Dibutyl phthalate induces oxidative stress and impairs spermatogenesis in adult rats. Toxicology and Industrial Health, 32(8), 1467–1477.
Anway, M. D., Memon, M. A., Uzumcu, M., and Skinner, M. K. (2006). Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. Journal of Andrology, 27(6), 868–879.
Arruzazabala, M. L., Pérez, Y., Ravelo, Y., Molina, V., Carbajal, D., Mas, R., and Rodríguez, E. (2011). Effect of oleic, lauric and myristic acids on phenylephrine-induced contractions of isolated rat vas deferens. Indian Journal of Experimental Biology, 49(9), 684–688.
Axelstad, M., Hass, U., Scholze, M., Christiansen, S., Kortenkamp, A., and Boberg, J. (2018). EDC impact: Reduced sperm counts in rats exposed to human-relevant mixtures of endocrine disrupters. Endocrine Connections, 7(1), 139–148.
Bar-El, D. S., and Reifen, R. (2010). Soy as an endocrine disruptor: Cause for caution? Journal of Pediatric Endocrinology and Metabolism, 23(9), 855–861.
Bindhumol, V., Chitra, K. C., and Mathur, P. P. (2003). Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology, 188(2–3), 117–124.
Blystone, C. R., Lambright, C. S., Cardon, M. C., Furr, J., Rider, C. V., Hartig, P. C., Wilson, V. S., and Gray, L. E. Jr. (2009). Cumulative and antagonistic effects of a mixture of the antiandrogens vinclozolin and iprodione in the pubertal male rat. Toxicological Sciences, 111(1), 179–188.
Cooper, T. G., Noonan, E., von Eckardstein, S., Auger, J., Baker, H. W. G., Behre, H. M., Haugen, T. B., Kruger, T., Wang, C., Mbizvo, M. T., and Vogelsong, K. M. (2010). World health organization reference values for human semen characteristics. Human Reproduction Update, 16(3), 231–245.
Doshi, T., Mehta, S. S., Dighe, V., Balasinor, N., and Vanage, G. (2011). Hypermethylation of estrogen receptor promoter region in adult testis of rats exposed neonatally to bisphenol A. Toxicology, 289(2–3), 74–82.
Enangue Njembele, A. N., Bailey, J. L., and Tremblay, J. J. (2014). In vitro exposure of Leydig cells to an environmentally relevant mixture of organochlorines represses early steps of steroidogenesis. Biology of Reproduction, 90(6), 118.
Esmaeili, V., Shahverdi, A. H., Moghadasian, M. H., and Alizadeh, A. R. (2015). Dietary fatty acids affect semen quality: A review. Andrology, 3(3), 450–461.
Feki, N. C., Abid, N., Rebai, A., Sellami, A., Ayed, B. B., Guermazi, M., Bahloul, A., Rebai, T., and Ammar, L. K. (2009). Semen quality decline among men in infertile relationships: Experience over 12 years in the South of Tunisia. Journal of Andrology, 30(5), 541–547.
Foster, P. M. (2006). Disruption of reproductive development in male rat offspring following in utero exposure to phthalate esters. International Journal of Andrology, 29(1), 140–147.
Giampietri, C., Petrungaro, S., Coluccia, P., D’Alessio, A., Starace, D., Riccioli, A., Padula, F., Palombi, F., Ziparo, E., Filippini, A., and De Cesaris, P. (2005). Germ cell apoptosis control during spermatogenesis. Contraception, 72(4), 298–302.
Henley, D. V., and Korach, K. S. (2010). Physiological effects and mechanisms of action of endocrine disrupting chemicals that alter estrogen signaling. Hormones, 9(3), 191–205.
Higuchi, T. T., Palmer, J. S., Gray, L. E., Jr., and Veeramachaneni, D. N. R. (2003). Effects of dibutyl phthalate in male rabbits following in utero, adolescent, or postpubertal exposure. Toxicological Sciences, 72(2), 301–313.
Kabuto, H., Amakawa, M., and Shishibori, T. (2004). Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sciences, 74(24), 2931–2940.
Kavlock, R. J., Dastron, G. P., Derosa, C., Fenner-Crisp, P., and Gray, L. E. (1996). Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop. Environmental Health Perspectives, 104, 715–740.
Kefer, J. C., Agarwal, A., and Sabanegh, E. (2009). Role of antioxidants in the treatment of male infertility. International Journal of Urology, 16(5), 449– 457.
Kelce, W. R., Gray, L. E., and Wilson, E. M. (1998). Antiandrogens as environmental endocrine disruptors. Reproduction Fertility and Development, 10(1), 105–111.
Knez, J. (2013). Endocrine-disrupting chemicals and male reproductive health. Reproductive Biomedicine Online, 26(5), 440–448.
Liu, J., Shimizu, K., and Kondo, R. (2009). Anti-androgenic activity of fatty acids. Chemistry and Biodiversity, 6(4), 503–512.
Loeffler, K. I., and Peterson, R. E. (1999). Interactive effects of TCDD and p,p′-DDE on male reproductive tract development in utero and lactationally exposed rats. Toxicology and Applied Pharmacology, 154 (1), 28–39.
Marques-Pinto, A., and Carvalho, D. (2013). Human infertility: Are endocrine disruptors to blame? Endocrine Connections, 2(3), R15–R29.
Meerts, I. A. T. M., Hoving, S., van den Berg, J. H. J., Weijers, B. M., Swarts, H. J., van der Beek, E. M., Bergman, A., Koeman, J. H., and Brouwer, A. (2004). Effects of in utero exposure to 4-hydroxy-2,3,3,4,5-pentachlorobiphenyl (4-OH-CB107) on developmental landmarks, steroid hormone levels and female estrous cyclicity in rats. Toxicological Sciences, 82, 259–267.
Orton, F., Ermler, S., Kugathas, S., Rosivatz, E., Scholze, M., and Kortenkamp, A. (2014). Mixture effects at very low doses with combinations of anti-androgenic pesticides, antioxidants, industrial pollutant and chemicals used in personal care products. Toxicology and Applied Pharmacology, 278(3), 201–208.
Oyelowo, O., Okafor, C., Ajibare, A., Ayomidele, B., Dada, K., Adelakun, R., and Ahmed, B. (2019). Fatty acids in some cooking oils as agents of hormonal manipulation in a rat model of benign prostate cancer. Nigerian Journal of Physiological Sciences, 34(1), 69–75.
Oyelowo, O. T., and Bolarinwa, A. F. (2017). Developmental consequences of in utero exposure to omega-9 monounsaturated fatty acid and its sex-skewing potential in rats. Journal of African Association of Physiological Sciences, 5(2), 85–92.
Oyelowo, O. T., and Bolarinwa, A. F. (2020). Early-life exposure to omega-9 monounsaturated fatty acid results in gonadal regression and elevated stress levels in pubertal male rat. Songklanakarin Journal of Science and Technology, 42(6), 1248–1252.
Oyelowo, T., and Adegoke, O. (2016). DNA fragmentation and oxidative stress can compromise sperm motility and survival in late pregnancy exposure to omega-9 fatty acid in rats. Iranian Journal of Basic Medical Sciences, 19, 511–520.
Piccinin, E., Cariello, M., De Santis, S., Ducheix, S., Sabbà, C., Ntambi, J. M., and Moschetta, A. (2019). Role of oleic acid in the gut-liver axis: From diet to the regulation of its synthesis via stearoyl-CoA desaturase 1 (SCD1). Nutrients, 11(10), 2283.
Puppel, K., Kapusta, A., and Kuczyn´ska, B. (2015). The etiology of oxidative stress in the various species of animals, a review. Journal of the Science of Food and Agriculture, 95(11), 2179–2184.
Sindhu, S. R., Singh, I. (2022). Phytosterols: Physiological functions and therapeutic applications. In Bioactive Food Components Activity in Mechanistic Approach (Cazarin, C. B. B., Bicas, J. L., Pastore, G. M., and Junior, M. R. M., Eds.), pp. 223–238. London: Academic Press.
Sidorkiewicz, I., Zaręba, K., Wołczyński, S., and Czerniecki, J. (2017). Endocrine-disrupting chemicals-Mechanisms of action on male reproductive system. Toxicology and Industrial Health, 3(7), 601–609.
Singh, S., and Li, S. S.-L. (2012). Epigenetic effects of environmental chemicals bisphenol A and phthalates. International Journal of Molecular Sciences, 13(8), 10143–10153.
Smith, S. B., and Smith, D. R. (2016). Fats: Production and uses of animal fats. In Encyclopedia of Food and Health (Caballero, B., Finglas, P. M., and Toldrá, F., Eds.), pp. 604–608. London: Academic Press.
Sun, M., and Zigman, S. (1978). An improved spectrophotometric assay for superoxide dismutase based on epinephrine autoxidation. Analytical Biochemistry, 90(1), 81–89.
Sunderland, E. M., Hu, X. C., Dassuncao, C., Tokranov, A. K., Wagner, C. C., and Allen, J. G. (2019). A review of the pathways of human exposure to poly- and perfluoroalkyl substances (PFASs) and present understanding of health effects. Journal of Exposure Science and Environmental Epidemiology, 29(2), 131–147.
Svechnikov, K., Izzo, G., Landreh, L., Weisser, J., and Söder, O. (2010). Endocrine disruptors and Leydig cell function. Journal of Biomedicine and Biotechnology, 2010, 684504.
Tremblay, J. J. (2015). Molecular regulation of steroidogenesis in endocrine Leydig cells. Steroids, 103, 3–10.
Uchiyama, M., and Mihara, M. (1978). Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Analytical Biochemistry, 86(1), 271–278.
van Dooran, R., Liejdekker, C. M., and Handerson, P. T. (1978). Synergistic effects of phorone on the hepatotoxicity of bromobenzene and paracetamol in mice. Toxicology, 11(3), 225–233.
Walczak-Jedrzejowska, R., Wolski, J. K., and Slowikowska- Hilczer, J. (2013). The role of oxidative stress and antioxidants in male fertility. Central European Journal of Urology, 66(1), 60–67.
Xie, M., Bu, P., Li, F., Lan, S., Wu, H., Yuan, L., and Wang, Y. (2016). Neonatal bisphenol A exposure induces meiotic arrest and apoptosis of spermatogenic cells. Oncotarget, 7(9), 10606–10615.
Yamamoto, M., Shirai, M., Sugita, K., Nagai, N., Miura, Y., Mogi, R., Yamamoto, K., Tamura, A., and Arishima, K. (2003). Effects of maternal exposure to diethylstilbestrol on the development of the reproductive system and thyroid function in male and female rat offspring. The Journal of Toxicological Sciences, 28(5), 385–394.
Zhang, G.-L., Zhang, X.-F., Feng, Y.-M., Li, L., Huynh, E., Sun, X.-F., Sun, Z.-Y., and Shen, W. (2013). Exposure to bisphenol A results in a decline in mouse spermatogenesis. Reproduction Fertility and Development, 25(6), 847–859.