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Abstract
This study aimed to evaluate the immunoreproductive and endocrine effects of exogenous oleic acid in mature female Wistar rats on an unrestricted diet. Eighteen mature Wistar rats with normal oestrous cycles were randomly divided into three groups: a control group and two experimental groups (low-dose and high-dose), each consisting of six rats. For three weeks, the rats in the experimental groups received daily oral doses of oleic acid at either 500 mg/kg or 1000 mg/kg of body weight. In contrast, the control group received 0.5 ml of distilled water. After the treatment, the oestrous cyclicity, serum hormone levels, reproductive organ weights, and blood parameters were analysed through a full blood count. The results showed no significant changes (p > 0.05) in oestrous cyclicity, serum oestrogen, progesterone, or luteinizing hormone levels. However, there was a significant increase (p < 0.05) in the weight of the relative reproductive tract, as well as in the number of mid-cells and neutrophils. Conversely, there was a substantial decrease (p < 0.05) in the relative lymphocyte count. Overall, the research indicated that oleic acid does not influence oestrous cyclicity or levels of serum oestrogen, progesterone, and luteinizing hormone in rats on an unrestricted diet. However, it does appear to have immunoregulatory effects on inflammatory cells.
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References
- Baddela, V.S., Michaelis, M., Sharma, A., Plinski, C., Viergutz, T., and Vanselow, J. (2022). Estradiol production of granulosa cells is unaffected by the physiological mix of nonesterified fatty acids in follicular fluid. J. Biol. Chem., 298 (10):102477. https://doi.org/10.1016/j.jbc.2022.102477
- Burch, M., Vargas-Bello-Pérez, E., and Busato, S. (2020). Advances in fatty acids nutrition in dairy cows: from gut to cells and effects on performance. J. Anim. Sci., 8 (35): 567-600. https://doi.org/10.1186/s40104-020-00512-8
- Calder, P. C., Yaqoob, P., Thies, F., Wallace, F. A., and Miles, E. A. (2002). Fatty acids and lymphocyte functions. Br. J. Nutr., 87 (Suppl 1): S31-48. https://doi.org/10.1079/bjn2001455
- Churakov, M., Karlsson, J., Rasmussen, A. E., and Holtenius, K. (2021). Milk fatty acids as indicators of negative energy balance of dairy cows in early lactation. Anim., 15 (7): 100253. https://doi.org/10.1016/j.animal.2021.100253.
- Cora, M. C., Kooistra, L., and Travlos, G. (2015). Vaginal cytology of the laboratory rat and mouse: Review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicol. Pathol., 43 (6): 776-93. https://doi.org/10.1177/0192623315570339
- Faas, M. M., and De Vos, P. (2018). Innate immune cells in the placental bed in healthy pregnancy and preeclampsia. Placenta, 69: 125-33. https://doi.org/10.1016/j.placenta.2018.04.012.
- Herrera-Camacho, J., Soberano-Martinez, A., Orozco, D. K. E., Aguila, P. C., and Carlos, J. (2011). Effect of fatty acids on reproductive performance of ruminants. InTech, 3 (4): 56-73. doi: https://doi.org/10.5772/16938
- Huang, N., Chi, H., and Qiao, J. (2020). Role of regulatory T cells in regulating fetal-maternal immune tolerance in healthy pregnancies and reproductive diseases. Front. Immunol., 11:1023. https://doi.org/10.3389/fimmu.2020.01023
- Jahangirifar, M., Taebi, M., Nasr-Esfahani, M. H., Heidari-Beni, M., and Asgari, G. H. (2021). Dietary fatty acid intakes and the outcomes of assisted reproductive technique in infertile women. J. Reprod. Infertil., 22 (3):173-83. https://doi.org/10.18502/jri.v22i3.6718
- Meikle, A., De Sousa, J. C. C., Hanzalova, J., and Murray, D. K. (1996). Oleic acid inhibits cholesteryl esterase and cholesterol utilization for testosterone synthesis in mouse leydig cells. Metab., 45 (3): 293–99. https://doi.org/10.1016/s0026-0495(96)90281-4
- National Research Council (NRC). Guide for the Care and Use of Laboratory Animals. Eight Edition. The National Academic Press, Washington, DC, 220 pages. https://doi.org/10.17226/12910.
- Owens, W., Ashby, J., Odum, J., and Onyon, LT. (2003). The OECD program to validate the rat uterotrophic bioassay. Phase 2: dietary phytoestrogen analyses. Environ. Health Perspect., 111 (12):1559-67. https://doi.org/10.1289/ehp.5949
- 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. J. Afr. Assoc . Physiol. Sci., 5 (2): 85-92. Accessed 6 June 2024 from file:///C:/Users/hp/Downloads/ajol-file-journals_557_articles_164939_submission_proof_164939-6565-425857-1-10-20180115%20(1).pdf
- Passoni, M. T., Palu, G., Grechi, N., Amaral, B. A. S., Gomes, C., Rülker, C., Van Ravenzwaay, B., and Martino-Andrade, A. J.(2021). Uterotrophic and in vitro screening for (anti)estrogenic activity of dipyrone. Toxicol. Lett., 352: 1-8. https://doi.org/10.1016/j.toxlet.2021.09.004.
- Patel, S., Patel, S., Kotadiya, A., Patel, S., Shrimali, B., Joshi, N., Patel. T., Trivedi, H., Patel, J., Joharapurkar, A., and Jain, M. (2024). Age-related changes in hematological and biochemical profiles of Wistar rats. Lab. Anim. Res. 40: 7. https://doi.org/10.1186/s42826-024-00194-7
- Pompura, S. L., Wagner, A., Kitz, A., LaPerche, J., Yosef, N., Dominguez-Villar, M., and Hafler, D. A. (2021). Oleic acid induces tissue resident foxP3 regulatory T cell lineage stability and suppressive functions. J. Clin. Invest. 131(2): e138519. https://doi.org/10.1172/JCI138519
- Prom, C. M., Dos Santo, N. J. M., Newbold, J. R., and Lock, A. L. (2021). Abomasal infusion of oleic acid increases fatty acid digestibility and plasma insulin of lactating dairy cows. J. Dairy Sci., 104 (12): 12616-627. https://doi.org/10.3168/jds.2021-20954
- Renaud, S. J., Postovit, L., Macdonald-Goodfellow, S. K., McDonald, G. T., Caldwell, J. D., and Charles, H. (2005). Activated macrophages inhibit human cytotrophoblast invasiveness in vitro. Biol. Reprod., 73 (2): 237–43, https://doi.org/10.1095/biolreprod.104.038000
- Santa-María, C., López-Enríquez, S., Montserrat-de la Paz, S., Geniz, I., Reyes-Quiroz, M. E., Moreno, M., Palomares, F., Sobrino, F., and Alba, G. (2023). Update on anti-inflammatory molecular mechanisms induced by oleic acid. Nutr., 15 (1): 224. https://doi.org/10.3390/nu15010224
- Singletary, S. J., Kirsch, A. J., Watson, J., Karim, B. O., Huso, D. L., Hurn, P. D., and Murphy, S. J. (2005). Lack of correlation of vaginal impedance measurements with hormone levels in the rat. Contemp. Top. Lab. Anim. Sci., 44 (6), 37–42. Accessed 8 November 2024 from https://pmc.ncbi.nlm.nih.gov/articles/PMC1403319/
- Taha-Abdelaziz, K., Astill, J., Kulkarni, R. R., Read, L. R., Najarian, A., Farber, J. M, and Sharif, S. (2019). In vitro assessment of immunomodulatory and anti-Campylobacter activities of probiotic lactobacilli. Sci. Rep., 9 (1):17903. https://doi.org/10.1038/s41598-019-54494-3
- Tutunchi, H., Ostadrahimi, A., and Saghafi‐Asl M. (2020). The effects of diets enriched in monounsaturated oleic acid on the management and prevention of obesity: A systematic review of human intervention studies. Adv. Nutr., 11 (4): 864–77. https://doi.org/10.1093/advances/nmaa013
- Verlengia, R., Gorjao, R., Kanunfre, C. C., Bordin, S., Martins de Lima, T., and Curi, R. (2003). Effect of arachidonic acid on proliferation, cytokines production and pleiotropic genes expression in Jurkat cells—A comparison with oleic acid. Life Sci., 73 (23): 2939 - 2951. https://doi.org/10.1016/j.lfs.2003.04.003.
- Yenuganti, V. R., Viergutz, T., and Vanselow, J. (2016). Oleic acid induces specific alterations in the morphology, gene expression and steroid hormone production of cultured bovine granulosa cells. Gen. Comp. Endocrinol., 232: 134–44. https://doi.org/10.1016/j.ygcen.2016.04.020.
- Zhou, X., Mo, Z., Li, Y., Huang, L., Yu, S., Ge, L., Hu, Y., Shi, S., Zhang, L., Wang, L., Gao, L., Yang, G., and Chu, G. (2022). Oleic acid reduces steroidogenesis by changing the lipid type stored in lipid droplets of ovarian granulosa cells. J. Anim. Sci. Biotechnol., 13 (1): 27. https://doi.org/10.1186/s40104-021-00660-5
References
Baddela, V.S., Michaelis, M., Sharma, A., Plinski, C., Viergutz, T., and Vanselow, J. (2022). Estradiol production of granulosa cells is unaffected by the physiological mix of nonesterified fatty acids in follicular fluid. J. Biol. Chem., 298 (10):102477. https://doi.org/10.1016/j.jbc.2022.102477
Burch, M., Vargas-Bello-Pérez, E., and Busato, S. (2020). Advances in fatty acids nutrition in dairy cows: from gut to cells and effects on performance. J. Anim. Sci., 8 (35): 567-600. https://doi.org/10.1186/s40104-020-00512-8
Calder, P. C., Yaqoob, P., Thies, F., Wallace, F. A., and Miles, E. A. (2002). Fatty acids and lymphocyte functions. Br. J. Nutr., 87 (Suppl 1): S31-48. https://doi.org/10.1079/bjn2001455
Churakov, M., Karlsson, J., Rasmussen, A. E., and Holtenius, K. (2021). Milk fatty acids as indicators of negative energy balance of dairy cows in early lactation. Anim., 15 (7): 100253. https://doi.org/10.1016/j.animal.2021.100253.
Cora, M. C., Kooistra, L., and Travlos, G. (2015). Vaginal cytology of the laboratory rat and mouse: Review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicol. Pathol., 43 (6): 776-93. https://doi.org/10.1177/0192623315570339
Faas, M. M., and De Vos, P. (2018). Innate immune cells in the placental bed in healthy pregnancy and preeclampsia. Placenta, 69: 125-33. https://doi.org/10.1016/j.placenta.2018.04.012.
Herrera-Camacho, J., Soberano-Martinez, A., Orozco, D. K. E., Aguila, P. C., and Carlos, J. (2011). Effect of fatty acids on reproductive performance of ruminants. InTech, 3 (4): 56-73. doi: https://doi.org/10.5772/16938
Huang, N., Chi, H., and Qiao, J. (2020). Role of regulatory T cells in regulating fetal-maternal immune tolerance in healthy pregnancies and reproductive diseases. Front. Immunol., 11:1023. https://doi.org/10.3389/fimmu.2020.01023
Jahangirifar, M., Taebi, M., Nasr-Esfahani, M. H., Heidari-Beni, M., and Asgari, G. H. (2021). Dietary fatty acid intakes and the outcomes of assisted reproductive technique in infertile women. J. Reprod. Infertil., 22 (3):173-83. https://doi.org/10.18502/jri.v22i3.6718
Meikle, A., De Sousa, J. C. C., Hanzalova, J., and Murray, D. K. (1996). Oleic acid inhibits cholesteryl esterase and cholesterol utilization for testosterone synthesis in mouse leydig cells. Metab., 45 (3): 293–99. https://doi.org/10.1016/s0026-0495(96)90281-4
National Research Council (NRC). Guide for the Care and Use of Laboratory Animals. Eight Edition. The National Academic Press, Washington, DC, 220 pages. https://doi.org/10.17226/12910.
Owens, W., Ashby, J., Odum, J., and Onyon, LT. (2003). The OECD program to validate the rat uterotrophic bioassay. Phase 2: dietary phytoestrogen analyses. Environ. Health Perspect., 111 (12):1559-67. https://doi.org/10.1289/ehp.5949
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. J. Afr. Assoc . Physiol. Sci., 5 (2): 85-92. Accessed 6 June 2024 from file:///C:/Users/hp/Downloads/ajol-file-journals_557_articles_164939_submission_proof_164939-6565-425857-1-10-20180115%20(1).pdf
Passoni, M. T., Palu, G., Grechi, N., Amaral, B. A. S., Gomes, C., Rülker, C., Van Ravenzwaay, B., and Martino-Andrade, A. J.(2021). Uterotrophic and in vitro screening for (anti)estrogenic activity of dipyrone. Toxicol. Lett., 352: 1-8. https://doi.org/10.1016/j.toxlet.2021.09.004.
Patel, S., Patel, S., Kotadiya, A., Patel, S., Shrimali, B., Joshi, N., Patel. T., Trivedi, H., Patel, J., Joharapurkar, A., and Jain, M. (2024). Age-related changes in hematological and biochemical profiles of Wistar rats. Lab. Anim. Res. 40: 7. https://doi.org/10.1186/s42826-024-00194-7
Pompura, S. L., Wagner, A., Kitz, A., LaPerche, J., Yosef, N., Dominguez-Villar, M., and Hafler, D. A. (2021). Oleic acid induces tissue resident foxP3 regulatory T cell lineage stability and suppressive functions. J. Clin. Invest. 131(2): e138519. https://doi.org/10.1172/JCI138519
Prom, C. M., Dos Santo, N. J. M., Newbold, J. R., and Lock, A. L. (2021). Abomasal infusion of oleic acid increases fatty acid digestibility and plasma insulin of lactating dairy cows. J. Dairy Sci., 104 (12): 12616-627. https://doi.org/10.3168/jds.2021-20954
Renaud, S. J., Postovit, L., Macdonald-Goodfellow, S. K., McDonald, G. T., Caldwell, J. D., and Charles, H. (2005). Activated macrophages inhibit human cytotrophoblast invasiveness in vitro. Biol. Reprod., 73 (2): 237–43, https://doi.org/10.1095/biolreprod.104.038000
Santa-María, C., López-Enríquez, S., Montserrat-de la Paz, S., Geniz, I., Reyes-Quiroz, M. E., Moreno, M., Palomares, F., Sobrino, F., and Alba, G. (2023). Update on anti-inflammatory molecular mechanisms induced by oleic acid. Nutr., 15 (1): 224. https://doi.org/10.3390/nu15010224
Singletary, S. J., Kirsch, A. J., Watson, J., Karim, B. O., Huso, D. L., Hurn, P. D., and Murphy, S. J. (2005). Lack of correlation of vaginal impedance measurements with hormone levels in the rat. Contemp. Top. Lab. Anim. Sci., 44 (6), 37–42. Accessed 8 November 2024 from https://pmc.ncbi.nlm.nih.gov/articles/PMC1403319/
Taha-Abdelaziz, K., Astill, J., Kulkarni, R. R., Read, L. R., Najarian, A., Farber, J. M, and Sharif, S. (2019). In vitro assessment of immunomodulatory and anti-Campylobacter activities of probiotic lactobacilli. Sci. Rep., 9 (1):17903. https://doi.org/10.1038/s41598-019-54494-3
Tutunchi, H., Ostadrahimi, A., and Saghafi‐Asl M. (2020). The effects of diets enriched in monounsaturated oleic acid on the management and prevention of obesity: A systematic review of human intervention studies. Adv. Nutr., 11 (4): 864–77. https://doi.org/10.1093/advances/nmaa013
Verlengia, R., Gorjao, R., Kanunfre, C. C., Bordin, S., Martins de Lima, T., and Curi, R. (2003). Effect of arachidonic acid on proliferation, cytokines production and pleiotropic genes expression in Jurkat cells—A comparison with oleic acid. Life Sci., 73 (23): 2939 - 2951. https://doi.org/10.1016/j.lfs.2003.04.003.
Yenuganti, V. R., Viergutz, T., and Vanselow, J. (2016). Oleic acid induces specific alterations in the morphology, gene expression and steroid hormone production of cultured bovine granulosa cells. Gen. Comp. Endocrinol., 232: 134–44. https://doi.org/10.1016/j.ygcen.2016.04.020.
Zhou, X., Mo, Z., Li, Y., Huang, L., Yu, S., Ge, L., Hu, Y., Shi, S., Zhang, L., Wang, L., Gao, L., Yang, G., and Chu, G. (2022). Oleic acid reduces steroidogenesis by changing the lipid type stored in lipid droplets of ovarian granulosa cells. J. Anim. Sci. Biotechnol., 13 (1): 27. https://doi.org/10.1186/s40104-021-00660-5