Direct action of leptin, obestatin and ginkgo on hormone release by luteinised human ovarian granulosa cells
Alexander V. Sirotkin A * , Adam Tarko A , Zuzana Fabova A , Miloš Mlynček A , Jan Kotwica B , Saleh Alwasel C and Abdel Halim Harrath CA Constantine the Philosopher University in Nitra, Tr. A. Hlinku 1, 949 74 Nitra, Slovakia.
B Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Olsztyn, Poland.
C Department of Zoology, King Saud University, College of Science, Riyadh 11451, Saudi Arabia.
Reproduction, Fertility and Development 34(18) 1128-1134 https://doi.org/10.1071/RD22154
Published online: 31 October 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: The role of metabolic hormones, medicinal plants and their interrelationships in the control of human reproductive processes are poorly understood.
Aims: To examine how leptin, obestatin and ginkgo (Ginkgo biloba L.) affect human ovarian hormone release.
Methods: We analysed the influence of leptin and obestatin alone and in combination with ginkgo extract on cultured human ovarian granulosa cells. The release of progesterone (P), insulin-like growth factor I (IGF-I), oxytocin (OT) and prostaglandin F (PGF) were analysed by enzyme immunoassay and enzyme-linked immunosorbent assay.
Key results: Leptin addition promoted the release of all the measured hormones. Obestatin stimulated the release of P, IGF-I and OT and inhibited PGF output. Ginkgo suppressed P, IGF-I and OT and promoted PGF release. Furthermore, ginkgo changed the stimulatory action of leptin on PGF to an inhibitory one.
Conclusions: Leptin and obestatin are involved in the control of human ovarian hormone release and ginkgo influences their function.
Implications: Leptin and obestatin could be useful as stimulators of human ovarian cell functions. The suppressive influence of ginkgo on ovarian function should lead to the development of ginkgo-containing drugs.
Keywords: ginkgo, IGF-I, metabolic hormones, ovary, oxytocin, progesterone, prostaglandin F, reproductive health.
References
Andrews, CJ, Thomas, DG, Welch, MV, Yapura, J, and Potter, MA (2020). Monitoring ovarian function and detecting pregnancy in felids: a review. Theriogenology 157, 245–253.| Monitoring ovarian function and detecting pregnancy in felids: a review.Crossref | GoogleScholarGoogle Scholar |
Chatterjee, SS, Doelman, CJA, Nöldner, M, Biber, A, and Koch, E (2005). Influence of the Ginkgo extract EGb 761 on rat liver cytochrome P450 and steroid metabolism and excretion in rats and man. Journal of Pharmacy and Pharmacology 57, 641–650.
| Influence of the Ginkgo extract EGb 761 on rat liver cytochrome P450 and steroid metabolism and excretion in rats and man.Crossref | GoogleScholarGoogle Scholar |
Childs, GV, Odle, AK, MacNicol, MC, and MacNicol, AM (2021). The importance of leptin to reproduction. Endocrinology 162, bqaa204.
| The importance of leptin to reproduction.Crossref | GoogleScholarGoogle Scholar |
Ding, X, Kou, X, Zhang, Y, Zhang, X, Cheng, G, and Jia, T (2017). Leptin siRNA promotes ovarian granulosa cell apoptosis and affects steroidogenesis by increasing NPY2 receptor expression. Gene 633, 28–34.
| Leptin siRNA promotes ovarian granulosa cell apoptosis and affects steroidogenesis by increasing NPY2 receptor expression.Crossref | GoogleScholarGoogle Scholar |
D’Occhio, MJ, Baruselli, PS, and Campanile, G (2019). Influence of nutrition, body condition, and metabolic status on reproduction in female beef cattle: a review. Theriogenology 125, 277–284.
| Influence of nutrition, body condition, and metabolic status on reproduction in female beef cattle: a review.Crossref | GoogleScholarGoogle Scholar |
Elmazoudy, RH, and Attia, AA (2012). Efficacy of Ginkgo biloba on vaginal estrous and ovarian histological alterations for evaluating anti-implantation and abortifacient potentials in albino female mice. Birth Defects Research Part B: Developmental and Reproductive Toxicology 95, 444–459.
| Efficacy of Ginkgo biloba on vaginal estrous and ovarian histological alterations for evaluating anti-implantation and abortifacient potentials in albino female mice.Crossref | GoogleScholarGoogle Scholar |
Fabová, Z, Loncová, B, Mlynček, M, and Sirotkin, AV (2022a). Kisspeptin as autocrine/paracrine regulator of human ovarian cell functions: possible interrelationships with FSH and its receptor. Reproductive Biology 22, 100580.
| Kisspeptin as autocrine/paracrine regulator of human ovarian cell functions: possible interrelationships with FSH and its receptor.Crossref | GoogleScholarGoogle Scholar |
Fabová, Z, Tarko, A, Harrath, AH, Alwasel, S, Kotwica, J, and Sirotkin, AV (2022b). Tribulus terrestris can suppress the adverse effect of toluene on bovine and equine ovarian granulosa cells. Reproduction in Domestic Animals , .
| Tribulus terrestris can suppress the adverse effect of toluene on bovine and equine ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Gregoraszczuk, EŁ, and Rak-Mardyła, A (2013). Supraphysiological leptin levels shift the profile of steroidogenesis in porcine ovarian follicles toward progesterone and testosterone secretion through increased expressions of CYP11A1 and 17b-HSD: a tissue culture approach. Reproduction 145, 311–317.
| Supraphysiological leptin levels shift the profile of steroidogenesis in porcine ovarian follicles toward progesterone and testosterone secretion through increased expressions of CYP11A1 and 17b-HSD: a tissue culture approach.Crossref | GoogleScholarGoogle Scholar |
Karamouti, M, Kollia, P, Kallitsaris, A, Vamvakopoulos, N, Kollios, G, and Messinis, IE (2009). Modulating effect of leptin on basal and follicle stimulating hormone stimulated steroidogenesis in cultured human lutein granulosa cells. Journal of Endocrinological Investigation 32, 415–419.
| Modulating effect of leptin on basal and follicle stimulating hormone stimulated steroidogenesis in cultured human lutein granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Kumar, PA, Sivakumar, AVN, Pathipati, D, Chakravarthi, VP, Brahmaiah, KV, and Rao, VH (2019). Leptin induced in vitro development of ovarian follicles in sheep is related to the expression of P450 aromatase and steroidogenesis. Theriogenology 136, 1–6.
| Leptin induced in vitro development of ovarian follicles in sheep is related to the expression of P450 aromatase and steroidogenesis.Crossref | GoogleScholarGoogle Scholar |
Loncová, B, Fabová, Z, and Sirotkin, AV (2021). Involvement of obestatin, cyclin-dependent kinase and protein kinase C in control of feline ovarian cell viability and hormones release. Reproductive Biology 21, 100560.
| Involvement of obestatin, cyclin-dependent kinase and protein kinase C in control of feline ovarian cell viability and hormones release.Crossref | GoogleScholarGoogle Scholar |
Martins, KR, Haas, CS, Rovani, MT, Moreira, F, Goetten, Aé LF, Ferst, JG, Portela, VM, Duggavathi, R, Bordignon, V, Gonçalves, PBD, Gasperin, BG, and Lucia, T (2021). Regulation and function of leptin during ovarian follicular development in cows. Animal Reproduction Science 227, 106689.
| Regulation and function of leptin during ovarian follicular development in cows.Crossref | GoogleScholarGoogle Scholar |
Mesen, TB, and Young, SL (2015). Progesterone and the luteal phase: a requisite to reproduction. Obstetrics and Gynecology Clinics of North America 42, 135–151.
| Progesterone and the luteal phase: a requisite to reproduction.Crossref | GoogleScholarGoogle Scholar |
Mészárosová, M, Sirotkin, AV, Grossmann, R, Darlak, K, and Valenzuela, F (2008). The effect of obestatin on porcine ovarian granulosa cells. Animal Reproduction Science 108, 196–207.
| The effect of obestatin on porcine ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Prakash, BS, Meyer, HHD, Schallenberger, E, and an de Wiel, DF (1987). Development of sensitive enzymeimmunoassay (EIA) for progesterone determination in unextracted bovine plasma using the second antibody technique. Journal of Steroid Biochemistry 28, 623–627.
| Development of sensitive enzymeimmunoassay (EIA) for progesterone determination in unextracted bovine plasma using the second antibody technique.Crossref | GoogleScholarGoogle Scholar |
Romani, F, Lanzone, A, Tropea, A, Familiari, A, Scarinci, E, Sali, M, Delogu, G, Catino, S, and Apa, R (2012). In vitro effect of unacylated ghrelin and obestatin on human luteal cell function. Fertility and Sterility 97, 991–996.
| In vitro effect of unacylated ghrelin and obestatin on human luteal cell function.Crossref | GoogleScholarGoogle Scholar |
Sirotkin AV (2014) ‘Regulators of ovarian functions.’ 2nd edn. (Nova Science Publishers, Inc.: New York) p. 194.
Sirotkin, AV (2021). Potential effects of ginkgo (Ginkgo biloba, L.) on female reproduction. Reproductive Biology 21, 100568.
| Potential effects of ginkgo (Ginkgo biloba, L.) on female reproduction.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, and Grossmann, R (2007). Leptin directly controls proliferation, apoptosis and secretory activity of cultured chicken ovarian cells. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 148, 422–429.
| Leptin directly controls proliferation, apoptosis and secretory activity of cultured chicken ovarian cells.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, and Grossmann, R (2015). Interrelationship between feeding level and the metabolic hormones leptin, ghrelin and obestatin in control of chicken egg laying and release of ovarian hormones. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 184, 1–5.
| Interrelationship between feeding level and the metabolic hormones leptin, ghrelin and obestatin in control of chicken egg laying and release of ovarian hormones.Crossref | GoogleScholarGoogle Scholar |
Sirotkin AV, Kolesarova A (2022) ‘Environmental contaminants and medicinal plants action on female reproduction.’ 1st edn. (Academic Press, Elsevier Science Publishing Co Inc.: London-San Diego-Cambridge-Oxford) p. 436.
Sirotkin, AV, and Meszarosová, M (2010). Comparison of effects of leptin and ghrelin on porcine ovarian granulosa cells. Domestic Animal Endocrinology 39, 1–9.
| Comparison of effects of leptin and ghrelin on porcine ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, Mlyncek, M, Makarevich, AV, Florkovičová, I, and Hetényi, L (2008). Leptin affects proliferation-, apoptosis- and protein kinase A-related peptides in human ovarian granulosa cells. Physiological Research 57, 437–442.
| Leptin affects proliferation-, apoptosis- and protein kinase A-related peptides in human ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, Rafay, J, and Kotwica, J (2009). Leptin controls rabbit ovarian function in vivo and in vitro: possible interrelationships with ghrelin. Theriogenology 72, 765–772.
| Leptin controls rabbit ovarian function in vivo and in vitro: possible interrelationships with ghrelin.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, Pavlova, S, Tena-Sempere, M, Grossmann, R, Jiménez, MR, Rodriguez, JMC, and Valenzuela, F (2013). Food restriction, ghrelin, its antagonist and obestatin control expression of ghrelin and its receptor in chicken hypothalamus and ovary. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 164, 141–153.
| Food restriction, ghrelin, its antagonist and obestatin control expression of ghrelin and its receptor in chicken hypothalamus and ovary.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, Mészárosová, M, Harrath, AH, and Grossmann, R (2016). Obestatin directly controls chicken ovarian cell functions. Journal of Biological Regulators and Homeostatic Agents 30, 665–674.
Sirotkin, AV, Tarko, A, Kotwica, J, Alrezaki, A, and Harrath, AH (2020a). Interrelationships between metabolic hormones, leptin and ghrelin, and oil-related contaminants in control of oxytocin and prostaglandin F release by feline ovaries. Reproductive Biology 20, 254–258.
| Interrelationships between metabolic hormones, leptin and ghrelin, and oil-related contaminants in control of oxytocin and prostaglandin F release by feline ovaries.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, Alexa, R, and Harrath, AH (2020b). Puncturevine (Tribulus terrestris L.) affects the proliferation, apoptosis, and ghrelin response of ovarian cells. Reproductive Biology 20, 33–36.
| Puncturevine (Tribulus terrestris L.) affects the proliferation, apoptosis, and ghrelin response of ovarian cells.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, Tarko, A, Alexa, R, Fakova, A, Alwasel, S, and Harrath, AH (2020c). Bee pollens originating from different species have unique effects on ovarian cell functions. Pharmaceutical Biology 58, 1101–1106.
| Bee pollens originating from different species have unique effects on ovarian cell functions.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, Alexa, R, Alwasel, S, and Harrath, AH (2021). Fennel affects ovarian cell proliferation, apoptosis, and response to ghrelin. Physiological Research 70, 237–243.
| Fennel affects ovarian cell proliferation, apoptosis, and response to ghrelin.Crossref | GoogleScholarGoogle Scholar |
Štochmaľová, A, Kádasi, A, Alexa, R, Bauer, M, Harrath, AH, and Sirotkin, AV (2018). Direct effect of pholyphenol-rich plants, rooibos and ginkgo, on porcine ovarian cell functions. Journal of Animal Physiology and Animal Nutrition 102, e550–e557.
| Direct effect of pholyphenol-rich plants, rooibos and ginkgo, on porcine ovarian cell functions.Crossref | GoogleScholarGoogle Scholar |
Vilariño-García, T, Pérez-Pérez, A, Santamaría-López, E, Prados, N, Fernández-Sánchez, M, and Sánchez-Margalet, V (2020). Sam68 mediates leptin signaling and action in human granulosa cells: possible role in leptin resistance in PCOS. Endocrine Connections 9, 479–488.
| Sam68 mediates leptin signaling and action in human granulosa cells: possible role in leptin resistance in PCOS.Crossref | GoogleScholarGoogle Scholar |
Wójik-Gładysz, A, Szlis, M, Przybył, BJ, and Polkowska, J (2019). Obestatin may affect the GnRH/KNDy gene network in sheep hypothalamus. Research in Veterinary Science 123, 51–58.
| Obestatin may affect the GnRH/KNDy gene network in sheep hypothalamus.Crossref | GoogleScholarGoogle Scholar |
Zieba, DA, Amstalden, M, and Williams, GL (2005). Regulatory roles of leptin in reproduction and metabolism: a comparative review. Domestic Animal Endocrinology 29, 166–185.
| Regulatory roles of leptin in reproduction and metabolism: a comparative review.Crossref | GoogleScholarGoogle Scholar |