ORIGINAL PAPER
Influence of green tea constituents on cultured porcine luteinized granulosa cell functions
More details
Hide details
1
Constantine the Philosopher University in Nitra, 949 74 Nitra, Slovak Republic
2
Research Institute of Animal Production, Luzianky, 951 41, Slovak Republic
3
Slovak University of Agriculture, 949 76 Nitra, Slovak Republic
4
Friedrich-Loeffler-Institute, Mariensee, 31535 Neustadt, Germany
5
King Saud University, Riyadh 11451, Saudi Arabia
Publication date: 2019-03-15
Corresponding author
A. V. Sirotkin
Constantine the Philosopher University in Nitra, 949 74 Nitra, Slovak Republic
J. Anim. Feed Sci. 2019;28(1):41-51
KEYWORDS
TOPICS
ABSTRACT
The aim of the study was to examine the action of green tea polyphenols
(GTPP) and their main constituent, epigallocatechin-3-gallate (EGCG),
on porcine ovarian granulosa cells. For this purpose, the effect of GTPP and
EGCG on cultured porcine ovarian granulosa cell functions, including proliferation,
apoptosis, steroidogenesis and response to insulin-like growth factor I
(IGF-I) was examined. Proliferation (the accumulation of proliferating cell nuclear
antigen (PCNA) and cyclin B1), apoptosis (the accumulation of bax and caspase
3) and the release of steroid hormones (progesterone and testosterone)
were evaluated by using immunocytochemistry and enzyme immunoassay. The
addition of both GTPP and EGCG reduced the percentage of both PCNA- and
cyclin B1-positive cells, increased the proportion of cells containing bax and
caspase 3 and stimulated progesterone release. GTPP had a biphasic effect on
testosterone output – stimulating at dose 1 μg/ml and inhibiting at doses 10 and
100 μg/ml, whilst EGCG did not affect testosterone secretion. IGF-I, when
administered alone, promoted % of cells containing PCNA, suppressed bax
accumulation, and stimulated progesterone release (only at dose 100 ng/ml).
Testosterone release increased after the addition of IGF-I at 1 ng/ml, but decreased
after IGF-I addition at 10 or 100 ng/ml. Both GTPP and EGCG suppressed
or even reversed the effects of IGF-I on percentage of PCNA-positive
cells, bax, testosterone output, and promoted IGF-I action on progesterone
release. These observations suggested the inhibitory actions of green tea constituents on porcine ovarian granulosa cell functions were mediated through
various regulatory mechanisms: suppression of the ovarian cell cycle in the
S and G2 phases; promotion of cytoplasmic apoptosis; alteration of steroid
hormone release; and, predominantly, prevention of the action of the hormonal
stimulator IGF-I on ovarian cells. It can be also suggested that the major GTPP
effects may result from the presence of EGCG.
REFERENCES (38)
1.
Abdelrazek H.M.A., Helmy S.A., Elsayed D.H., Ebaid H.M., Mohamed R.M., 2016. Ameliorating effects of green tea extract on cadmium induced reproductive injury in male Wistar rats with respect to androgen receptors and caspase-3. Reprod. Biol. 16, 300–308,
https://doi.org/10.1016/j.repb....
2.
Basini G., Bianco F., Grasselli F., 2005. Epigallocatechin-3-gallate from green tea negatively affects swine granulosa cell function. Domest. Anim. Endocrinol. 28, 243–256,
https://doi.org/10.1016/j.doma....
3.
Bucci D., Spinaci M., Mislei B., Gadani B., Rizzato G., Love C.C., Tamanini C., Galeati G., Mari G., 2017. Epigallocatechin-3-gallate (EGCG) and green tea polyphenols do not improve stallion semen parameters during cooling at 4 °C. Reprod. Domest. Anim. 52, 270–277,
https://doi.org/10.1111/rda.12....
4.
Chandra A.K., Choudhury S.R., De N., Sarkar M., 2011. Effect of green tea (Camellia sinensis L.) extract on morphological and functional changes in adult male gonads of albino rats. Indian J. Exp. Biol. 49, 689–697.
6.
Das S.K., Karmakar S.N., 2015. Effect of green tea (Camellia sinensis L.) leaf extract on reproductive system of adult male albino rats. Int. J. Physiol. Pathophysiol. Pharmacol. 7, 178–184.
7.
Dias T.R., Alves M.G., Rato L., Casal S., Silva B.M., Oliveira P.F., 2016. White tea intake prevents prediabetes-induced metabolic dysfunctions in testis and epididymis preserving sperm quality. J. Nutr. Biochem. 37, 83–93,
https://doi.org/10.1016/j.jnut....
8.
Ding J., Wang H., Wu Z.-B., Zhao J., Zhang S., Li W., 2015. Protection of murine spermatogenesis against ionizing radiation-induced testicular injury by a green tea polyphenol. Biol. Reprod. 92, 6,
https://doi.org/10.1095/biolre....
9.
Figueiroa M.S., César Vieira J.S.B., Leite D.S., Andrade Filho R.C.O., Ferreira F., Gouveia P.S., Udrisar D.P., Wanderley M.I., 2009. Green tea polyphenols inhibit testosterone production in rat Leydig cells. Asian J. Androl. 11, 362–370,
https://doi.org/10.1038/aja.20....
10.
Ghafurniyan H., Azarnia M., Nabiuni M., Karimzadeh L., 2015. The effect of green tea extract on reproductive improvement in estradiol valerate-induced polycystic ovarian syndrome in rat. Iran. J. Pharm. Res. 14, 1215–1233.
11.
Hijazi M.M., Khatoon N., Azmi M.A., Rajput M.T., Zaidi S.I., Azmi M.A., Perveen R., Naqvi S.N., Rashid M., 2015. Report: effects of Camellia sinensis L. (green tea) extract on the body and testicular weight changes in adult Wistar rate. Pak. J. Pharm. Sci. 28, 249–253.
12.
Kádasi A., Maruniaková N., Štochmaľová A., Bauer M., Grossmann R., Harrath A.H., Kolesárová A., Sirotkin A.V., 2017. Direct effect of curcumin on porcine ovarian cell functions. Anim. Reprod. Sci. 182, 77–83,
https://doi.org/10.1016/j.anir....
13.
Kao Y.-H., Hiipakka R.A., Liao S., 2000. Modulation of endocrine systems and food intake by green tea epigallocatechin gallate. Endocrinology 141, 980–987,
https://doi.org/10.1210/endo.1....
14.
Kaplanoglu G.T., Bahcelioglu M., Gozil R., Helvacioglu F., Buru E., Tekindal M.A., Erdogan D., Calguner E., 2013. Effects of green tea and vitamin E in the testicular tissue of streptozotocin-induced diabetic rats. Saudi Med. J. 34, 734–743.
15.
Karran L., Dyer M.J.S., 2001. Proteolytic cleavage of molecules involved in cell death or survival pathways: a role in the control of apoptosis? Crit. Rev. Eukaryot. Gene Expr. 11(4),
https://doi.org/10.1615/CritRe....
16.
Kulandaivelu K., Mandal A.K.A., 2017. Improved bioavailability and pharmacokinetics of tea polyphenols by encapsulation into gelatin nanoparticles. IET Nanobiotechnol. 11, 469–476,
https://doi.org/10.1049/iet-nb....
17.
Law F.C.P., Yao M., Bi H.-C., Lam S., 2017. Physiologically based pharmacokinetic modeling of tea catechin mixture in rats and humans. Pharmacol. Res. Perspect. 5, e00305,
https://doi.org/10.1002/prp2.3....
18.
Liebermann D.A., Hoffman B., 2007. Gadd45 in the response of hematopoietic cells to genotoxic stress. Blood Cells Mol. Dis. 39, 329–335,
https://doi.org/10.1016/j.bcmd....
19.
Mészárosová M., Sirotkin A.V., Grossmann R., Darlak K., Valenzuela F., 2008. The effect of obestatin on porcine ovarian granulosa cells. Anim. Reprod. Sci. 108, 196–207,
https://doi.org/10.1016/j.anir....
20.
Münster E., 1989. Development of enzyme immunological measuring methods on microtitration plates for the determination of testosterone and progesterone in blood plasma (in German). Thesis. Institute for Animal Production and Breeding of the University of Hohemheim. Stuttgart (Germany), pp. 154.
21.
Naryzhny S.N., Lee H., 2001. Protein profiles of the Chinese hamster ovary cells in the resting and proliferating stages. Electrophoresis 22, 1764–1775,
https://doi.org/10.1002/1522-2...<1764::AID-ELPS1764>3.0.CO;2-V.
22.
Niedzwiecki A., Roomi M.W., Kalinovsky T., Rath M., 2016. Anticancer efficacy of polyphenols and their combinations. Nutrients. 8, 552,
https://doi.org/10.3390/nu8090....
23.
Oliveira P.F., Tomás G.D., Dias T.R., Martins A.D., Rato L., Alves M.G., Silva B.M., 2015. White tea consumption restores sperm quality in prediabetic rats preventing testicular oxidative damage. Reprod. Biomed. Online 31, 5445–5456,
https://doi.org/10.1016/j.rbmo....
24.
Prakash B.S., Meyer H.H.D., Schallenberger E., van De Wiel D.F.M., 1987. Development of a sensitive enzymeimmunoassay (EIA) for progesterone determination in unextracted bovine plasma using the second antibody technique. J. Steroid Biochem. 28, 623–627,
https://doi.org/10.1016/0022-4....
25.
Quirk S.M., Cowan R.G., Harman R.M., Hu C.-L., Porter D.A., 2004. Ovarian follicular growth and atresia: the relationship between cell proliferation and survival. J. Anim. Sci. 82, Suppl. 13, E40–E52,
https://doi.org/10.2527/2004.8....
26.
Roychoudhury S., Agarwal A., Virk G., Cho C.-L., 2017. Potential role of green tea catechins in the management of oxidative stressassociated infertility. Reprod. Biomed. Online 34, 487–498,
https://doi.org/10.1016/j.rbmo....
27.
Roychoudhury S., Halenar M., Michalcova K., Nath S., Kacaniova M., Kolesarova A., 2018. Green yea extract affects porcine ovarian cell apoptosis. Reprod. Biol. 18, 94–98,
https://doi.org/10.1016/j.repb....
28.
Saeed M., Naveed M., Arif M. et al., 2017. Green tea (Camellia sinensis) and L-theanine: Medicinal values and beneficial applications in humans – A comprehensive review. Biomed. Pharmacother. 95, 1260–1275,
https://doi.org/10.1016/j.biop....
29.
Sharma P., Goyal P.K., 2015. Ameliorative effect of green tea catechin against cadmium chloride-induced testicular toxicity in mice. J. Environ. Pathol. Toxicol. Oncol. 34, 335–352,
https://doi.org/10.1615/JEnvir....
30.
Sirotkin A.V., 2010. Effect of two types of stress (heat shock/high temperature and malnutrition/serum deprivation) on porcine ovarian cell functions and their response to hormones. J. Exp. Biol. 213, 2125–2130,
https://doi.org/10.1242/jeb.04....
31.
Sirotkin A.V., 2014. Regulators of Ovarian Functions. Nova Publishers, Inc. New York, NY (USA), pp. 194.
34.
Spinaci M., Volpe S., De Ambrogi M., Tamanini C., Galeati G., 2008. Effects of epigallocatechin-3-gallate (EGCG) on in vitro maturation and fertilization of porcine oocytes. Theriogenology 69, 877–885,
https://doi.org/10.1016/j.ther....
35.
Štochmaľová A., Kádasi A., Alexa R., Bauer M., Harrath A.H., Sirotkin A.V., 2018. Direct effect of pholyphenol-rich plants, rooibos and ginkgo, on porcine ovarian cell functions. J. Anim. Physiol. Anim. Nutr. 102, e550–e557,
https://doi.org/10.1111/jpn.12....
36.
Wang Z.-g., Yu S.-d., Xu Z.-r., 2007. Improvement in bovine embryo production in vitro by treatment with green tea polyphenols during in vitro maturation of oocytes. Anim. Reprod. Sci. 100, 22–31,
https://doi.org/10.1016/j.anir....
37.
Wein S., Beyer B., Gohlke A., Blank R., Metges C.C., Wolffram S., 2016. Systemic absorption of catechins after intraruminal or intraduodenal application of a green tea extract in cows. PLoS ONE 11, e0159428,
https://doi.org/10.1371/journa....
38.
Zheng J.H., Viacava Follis A., Kriwacki R.W., Moldoveanu T., 2016. Discoveries and controversies in BCL-2 protein-mediated apoptosis. FEBS J. 283, 2690–2700,
https://doi.org/10.1111/febs.1....
CITATIONS (1):
1.
Environmental Contaminants and Medicinal Plants Action on Female Reproduction
Alexander Sirotkin, Adriana Kolesarova