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Current Drug Therapy

Editor-in-Chief

ISSN (Print): 1574-8855
ISSN (Online): 2212-3903

Research Article

Plumeria acuminata: A Systematic In Vivo Evaluation for its Antiovulatory and Anti-implantation Features

Author(s): Jay P. Rabadia*, Tushar R. Desai and Vihang S. Thite

Volume 17, Issue 3, 2022

Published on: 22 June, 2022

Page: [186 - 207] Pages: 22

DOI: 10.2174/1574885517666220426101516

Price: $65

Abstract

Background: Fertility control becomes necessary for under-developed and developing nations for the betterment of the economy, environment, and society. Plant Plumeria acuminata, “Temple tree or Frangipani,” of the Apocynaceae family, has exhibited several activities similar to contraceptive medicine and is widely distributed in India.

Objective: Present investigation aimed to study the anti-ovulatory and anti-implantation activities of ethanolic extract from P. acuminata leaves and roots in Wistar rats.

Methods: Ethanolic extracts of P. acuminata leaves and roots were subjected to qualitative phytochemical analysis and acute toxicity test. Immature female rats were used to explore anti-ovulatory characteristics by administering HCG as a standard ovulation-inducing drug. Mated females were used for exploring anti-implantation characteristics. Levonorgestrel and Ethinylestradiol were administered as standard anti-implantation drugs. Morphological, hematological, hormonal, and histological examinations were performed.

Results: LD50 value, i.e., 2000 mg/kg from acute toxicity test, resulted in the selection of 100, 200, and 400 mg/kg dose values for both leaf and root extracts. Treatment with these brought ~2-54%, ~5- 48%, and ~1-68% changes respectively in the hormonal, growth factors’ and cytokines’ profiles. Ovarian histology revealed restricted follicle maturation and ovulation, whereas uterine histology unveiled a ~5-28% decrease in the endometrium thickness, making it unreceptive for implantation after treatment with PAL and PAR extracts.

Conclusion: Anti-ovulatory and anti-implantation results obtained here can be attributed to the presence of plumericin, sterol, as well as triterpene groups of phytochemicals from ethanolic extracts of leaves and roots, making them potent contestants for studies on future contraceptive medicines.

Keywords: Anti-ovulatory, anti-implantation, hormone, growth factor, cytokine, fertility, contraceptive.

Graphical Abstract

[1]
Devi P, Kumar P, Dhamija N, Dhamija I. Antifertility activity of medicinal plants on male and female reproduction. Int J Pharm Sci Res 2015; 6(3): 988-1001.
[2]
Bhatt N, Deshpande M. A Critical review and scientific perspective on contraceptive therapeutics from Ayurveda and allied ancient knowledge. Front Pharmacol 2021; 12: 629591.
[http://dx.doi.org/10.3389/fphar.2021.629591] [PMID: 34149405]
[3]
Khan F, Mukhtar S, Dickinson IK, Sriprasad S. The story of the condom. Indian J Urol 2013; 29(1): 12-5.
[http://dx.doi.org/10.4103/0970-1591.109976] [PMID: 23671357]
[4]
Chakraverty R, Sasmal S. A Systematic review on natural based anti-fertility drugs. Acta Sci Pharm Sci 2018; 2(12): 35-40.
[5]
Mark-Kappeler CJ, Sen N, Keating AF, Sipes IG, Hoyer PB. Distribution and responsiveness of rat anti-Müllerian hormone during ovarian development and VCD-induced ovotoxicity. Toxicol Appl Pharmacol 2010; 249(1): 1-7.
[http://dx.doi.org/10.1016/j.taap.2010.08.024] [PMID: 20816688]
[6]
Sela-Abramovich S, Galiani D, Nevo N, Dekel N. Inhibition of rat oocyte maturation and ovulation by nitric oxide: Mechanism of action. Biol Reprod 2008; 78(6): 1111-8.
[http://dx.doi.org/10.1095/biolreprod.107.065490] [PMID: 18337515]
[7]
Kim S-M, Kim J-S. A Review of mechanisms of implantation. Dev Reprod 2017; 21(4): 351-9.
[http://dx.doi.org/10.12717/DR.2017.21.4.351] [PMID: 29359200]
[8]
Achache H, Revel A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update 2006; 12(6): 731-46.
[http://dx.doi.org/10.1093/humupd/dml004] [PMID: 16982667]
[9]
Diedrich K, Fauser BCJM, Devroey P, Griesinger G. The role of the endometrium and embryo in human implantation. Hum Reprod Update 2007; 13(4): 365-77.
[http://dx.doi.org/10.1093/humupd/dmm011] [PMID: 17548368]
[10]
Amjadi F, Aflatoonian R, Javanmard SH, Saifi B, Ashrafi M, Mehdizadeh M. Apolipoprotein A1 as a novel anti-implantation biomarker in polycystic ovary syndrome: A case-control study. J Res Med Sci 2015; 20(11): 1039-45.
[http://dx.doi.org/10.4103/1735-1995.172813] [PMID: 26941806]
[11]
Makrigiannakis A, Minas V. Mechanisms of implantation. Reprod Biomed Online 2007; 14(1): 102-9.
[http://dx.doi.org/10.1016/S1472-6483(10)60771-7] [PMID: 17207342]
[12]
van Mourik MSM, Macklon NS, Heijnen CJ. Embryonic implantation: Cytokines, adhesion molecules, and immune cells in establishing an implantation environment. J Leukoc Biol 2009; 85(1): 4-19.
[http://dx.doi.org/10.1189/jlb.0708395] [PMID: 18784344]
[13]
Yadav M, Singh DP, Verma C, Singh S, Saini A, Dubey A. Development of multicomponent herbal formulation and its evaluation for antifertility activity. Int J Pharm Phytopharmacol Res 2013; 2(4): 277-82.
[14]
Feroche AT. Evaluation of abortifacient efficacy of Rumex steudelli (Tult) root traditionally used medicinal plant in South West Ethiopia. Phytopharm 2015; 4(4): 221-3.
[http://dx.doi.org/10.31254/phyto.2015.4406]
[15]
Lee HJ, Macbeth AH, Pagani JH, Young WS III. Oxytocin: The great facilitator of life. Prog Neurobiol 2009; 88(2): 127-51.
[PMID: 19482229]
[16]
Ishak WW, Kahloon M, Fakhry H. Oxytocin role in enhancing well-being: A literature review. J Affect Disord 2011; 130(1-2): 1-9.
[http://dx.doi.org/10.1016/j.jad.2010.06.001] [PMID: 20584551]
[17]
Airaodion AI, Okoroukwu VN, Ogbuagu EO, Ogbuagu U. In vitro and in vivo evaluation of Ananas comosus fruit (pineapple) on abortion/miscarriage in Wistar rats. Int J BioSci Biotechnol 2019; 11(9): 69-75.
[18]
Kharkwal G, Fatima I, Kitchlu S, Singh B, Hajela K, Dwivedi A. Anti-implantation effect of 2-[piperidinoethoxyphenyl]-3-[4-hydroxyphenyl]-2H-benzo(b)pyran, a potent antiestrogenic agent in rats. Fertil Steril 2011; 95(4): 1322-7.
[http://dx.doi.org/10.1016/j.fertnstert.2010.06.066] [PMID: 20674906]
[19]
Bala K, Arya M, Pandey Katare D. Herbal contraceptive: An overview. World J Pharm Pharm Sci 2014; 3(8): 1305-26.
[20]
Gomathi P, Shalini T, Farheen N, Sanjeevkumar A. Antidiabetic activity of Plumeria acuminata leaves on streptozotocin-induced diabetic rats. Asian J Res Biol Pharm Sci 2016; 4(3): 99-104.
[21]
Prakash D, Tembare R, Gurav S, Kumar SG, Tamizh Mani T. An review of phytochemical constituents and pharmacological activity of Plumeria species. Int J Curr Pharm Res 2012; 4(1): 1-6.
[22]
Chandra Taid T, Ch Rajkhowa R, Ch Kalita J. The effect of Plumeria acuminata ait on oestrous cycle and acute oral toxicity study in c3h female albino mice. Int J Dev Res 2016; 6(12): 10620-4.
[23]
Farooque A, Mazumder A, Shambhawee S, Mazumder R. Review on Plumeria acuminata. Int J Res Pharm Chem 2012; 2(2): 467-9.
[24]
Singh R, Kakar S, Shah M, Jain R. Some medicinal plants with anti-fertility potential: A current ctatus. J Basic Clin Reprod Sci 2018; 7(1): 7-19.
[25]
Gupta M, Mazumdar UK, Gomathi P. Evaluation of antipyretic and antinociceptive activities of Plumeria acuminata Leaves. J Med Sci 2007; 7(5): 835-9.
[http://dx.doi.org/10.3923/jms.2007.835.839]
[26]
Sunitha K, Naga Rani C. Antibacterial activity of methanolic extracts of flowers of Plumeria acuminata. J Glob Trends Pharm Sci 2018; 9(1): 4978-80.
[27]
Yadav A, Undale V, Bhosale A. Antidiabetic activity of Plumeria rubra L. in normal and alloxan induced diabetic mice. Int J Basic Clin Pharmacol 2016; 5(3): 884-9.
[http://dx.doi.org/10.18203/2319-2003.ijbcp20161540]
[28]
Periyasamy G, Gupta M, Mazumder UK, Gebrelibanos M, Sintayehu B. Antioxidant and antitumor activity of Plumeria acuminata in ehrlich ascites carcinoma bearing swiss albino mice. Br J Pharm Res 2013; 3(4): 671-85.
[http://dx.doi.org/10.9734/BJPR/2013/4472]
[29]
Gupta M. Phytochemical screening of leaves of Plumeria alba and Plumeria acuminata. J Chem Pharm Res 2016; 8(5): 354-8.
[30]
Ali H, Dixit S, Ali D, Alqahtani SM, Alkahtani S, Alarifi S. Isolation and evaluation of anticancer efficacy of stigmasterol in a mouse model of DMBA-induced skin carcinoma. Drug Des Devel Ther 2015; 9: 2793-800.
[http://dx.doi.org/10.2147/DDDT.S83514] [PMID: 26060396]
[31]
Rajeswari K, Bhaskara Rao T, Krishna MR. Anti-cancer activity of stigmasterol of Xylocarpus granatum in cytotoxicity studies using Hela And Mcf-7 cells. Org Med Chem Int J 2018; 7(4): 1-5.
[32]
Kangsamaksin T, Chaithongyot S, Wootthichairangsan C, Hanchaina R, Tangshewinsirikul C, Svasti J. Lupeol and stigmasterol suppress tumor angiogenesis and inhibit cholangiocarcinoma growth in mice via downregulation of tumor necrosis factor-α. PLoS One 2017; 12(12): e0189628.
[http://dx.doi.org/10.1371/journal.pone.0189628] [PMID: 29232409]
[33]
Ghosh A, Bose S, Chakraborti CK. Anti-inflammatory, antipyretic and analgesic properties of extracts and isolated stigmasterol from Cucurbita maxima seeds. Proceedings of the SPER International Conference. 2019 June 7-8; Nepal: Kathmandu University 2019.
[34]
Ullah R, Alsaid MS, Alqahtani AS, et al. Anti-inflammatory, antipyretic, analgesic, and antioxidant activities of Haloxylon salicornicum aqueous fraction. Open Chem 2019; 17(1): 1034-42.
[http://dx.doi.org/10.1515/chem-2019-0113]
[35]
Yuan L, Zhang F, Shen M, Jia S, Xie J. Phytosterols suppress phagocytosis and inhibit inflammatory mediators via ERK pathway on LPS-triggered inflammatory responses in RAW264. 7 macrophages and the correlation with their structure. Foods 2019; 8(11): 582.
[http://dx.doi.org/10.3390/foods8110582] [PMID: 31744147]
[36]
Malladi S, Ratnakaram VN, Babu S. Phytochemical Investigation of Caralluma lasiantha: Isolation of stigmastserol, an active immunomodulatory agent. Int J Chem Sci 2017; 15(1): 399-407.
[37]
Khanam S, Sultana R. Isolation of β-sitosterol & stigmasterol as active immunomodulatory constituents from fruits of Solanum xanthocarpum (solanaceae). Int J Pharm Sci Res 2012; 3(4): 1057-60.
[38]
Jivrajani M, Ravat N, Anandjiwala S, Nivsarkar M. Antiestrogenic and anti-Inflammatory potential of n -Hexane fraction of Vitex negundo Linn leaf extract: A probable mechanism for blastocyst implantation failure in Mus musculus. Int Sch Res Notices 2014; 2014: 241946.
[http://dx.doi.org/10.1155/2014/241946] [PMID: 27351007]
[39]
Liang S, Shen YH, Feng Y, et al. Terpenoids from Daphne aurantiaca and their potential anti-inflammatory activity. J Nat Prod 2010; 73(4): 532-5.
[http://dx.doi.org/10.1021/np9005053] [PMID: 20192236]
[40]
Cheng AYF, Teoh PL, Jayasinghe L, Cheong BE. Volatile profiling aided in the isolation of anti-proliferative lupeol from the roots of Clinacanthus nutans (Burm. f.) lindau. Processes (Basel) 2021; 9(1383): 1-14.
[http://dx.doi.org/10.3390/pr9081383]
[41]
Newill H, Loske R, Wagner J, Johannes C, Lorenz RL, Lehmann L. Oxidation products of stigmasterol interfere with the action of the female sex hormone 17β-estradiol in cultured human breast and endometrium cell lines. Mol Nutr Food Res 2007; 51(7): 888-98.
[http://dx.doi.org/10.1002/mnfr.200700025] [PMID: 17579897]
[42]
Jerald SE, Pandey A, Bigoniya P, Singh S. Antifertility activity of Momordica charantia descourt pulp and seed hydroalcoholic extract. J App Pharm 2012; 03(04): 682-96.
[43]
Min J, Cao L, Zhou J, Wu X, Li L. Plumericin inhibits growth of liver carcinoma cells via downregulation of COX-2 and VEGF. Trop J Pharm Res 2018; 17(12): 2387-92.
[http://dx.doi.org/10.4314/tjpr.v17i12.11]
[44]
Fakhrudin N, Waltenberger B, Cabaravdic M, et al. Identification of plumericin as a potent new inhibitor of the NF-κB pathway with anti-inflammatory activity in vitro and in vivo. Br J Pharmacol 2014; 171(7): 1676-86.
[http://dx.doi.org/10.1111/bph.12558] [PMID: 24329519]
[45]
Marin AR, Roco IM, Okanya VK, Olin NC, Jewel J, Pancho E. Bronchodilation effects of kalachuchi leaves (Plumeria acuminata, family: Apocynaceae) of ethanol extracts on cat-induced bronchoconstriction. Eur J Pharm Med Res 2020; 7(1): 15-29.
[46]
Hyacinth AA, Nwocha UC. Antifertility activity of aqueous ethanolic extract of Hymenocardia acida stem bark in female rats. Iran J Reprod Med 2011; 9(3): 217-22.
[PMID: 26396567]
[47]
Kumar Shah S, Jhade D, Chouksey R. Antifertility activity of ethanolic and aqueous extracts of Aloe vera Mill on female wistar rats: Rising approaches of herbal contraception. J Pharm Sci Res 2016; 8(9): 952-7.
[48]
Jaber BM, Jasim SF. Phytochemical study of stigmasterol and β-sitosterol in Viola odorata plant cultivated in Iraq. Iran J Biotechnol 2014; 13(2): 86-94.
[49]
Edwin S, Balkrishna JS, Chand JD. Antifertility activity of stems of Plumbago zeylanica Linn. in female albino rats. 2008. Iran J Pharmacol Ther 2008; 7(2): 169-74.
[50]
Jain S, Choudhary GP, Jain DK. Pharmacological evaluation and antifertility activity of Jatropha gossypifolia in rats. BioMed Res Int 2013; 2013: 125980.
[http://dx.doi.org/10.1155/2013/125980] [PMID: 24222894]
[51]
Ahirwar D, Ahirwar B, Kharya MD. Evaluation of antifertility activity of Trigonella foenum graecum seeds. Pharm Sin 2010; 1(3): 33-9.
[52]
Kon H, Hokao R, Shinoda M. Fertilizability of superovulated eggs by estrous stage-independent PMSG/hCG treatment in adult Wistar-Imamichi rats. Exp Anim 2014; 63(2): 175-82.
[http://dx.doi.org/10.1538/expanim.63.175] [PMID: 24770643]
[53]
Kachroo M. Isolation, characterisation and anti-fertility activity of the active moiety from the seeds of Ensete superbum cheesm (Banakadali). J Nat Rem 2009; 9(1): 12-20.
[54]
Simone J, Bogue EA, Bhatti DL, et al. Ethinyl estradiol and levonorgestrel alter cognition and anxiety in rats concurrent with a decrease in tyrosine hydroxylase expression in the locus coeruleus and brain-derived neurotrophic factor expression in the hippocampus. Psychoneuroendocrinology 2015; 62: 265-78.
[http://dx.doi.org/10.1016/j.psyneuen.2015.08.015] [PMID: 26352480]
[55]
OECD. Test No.423: Acute oral toxicity-Acute toxic class method. 2002; 1-14. Available from: https://www.oecd-ilibrary.org/environ ment/test-no-423-acute-oral-toxicity-acute-toxic-class
[56]
Rafert S, Mariot J, Klett D, Combarnous Y. Involvement of ovarian estradiol biosynthesis and pituitary FSH expression in the mechanism of human chorionic gonadotropin stimulation of uterine growth in immature female rats. J Hormones 2016; 2016: 6923239.
[57]
Gaytan M, Bellido C, Morales C, Gonzalez-Padilla M, Sanchez-Criado JE, Gaytan F. Immature rats show ovulatory defects similar to those in adult rats lacking prostaglandin and progesterone actions. Reprod Biol Endocrinol 2004; 2(1): 63.
[http://dx.doi.org/10.1186/1477-7827-2-63] [PMID: 15345060]
[58]
Smitz J, Platteau P. Influence of human chorionic gonadotrophin during ovarian stimulation: An overview. Reprod Biol Endocrinol 2020; 18(1): 80.
[http://dx.doi.org/10.1186/s12958-020-00639-3] [PMID: 32762698]
[59]
Rani S. Preliminary study on the anti-implantation activity of Leptadenia reticulata in female rats. Int J Pharm Tech Res 2009; 1(4): 1403-5.
[60]
Okoko IIE, Osinubi AAA, Olabiyi OO, Kusemiju TO, Noronha CC, Okanlawon AO. Antiovulatory and anti-implantation potential of the methanolic extract of seeds of Abrus precatorius in the rat. Endocr Pract 2010; 16(4): 554-60.
[http://dx.doi.org/10.4158/EP09011.OR] [PMID: 20150030]
[61]
Koneri R, Saraswati CD, Balaraman R, Ajeesha EA. Antiimplantation activity of the ethanolic root extract of Momordica cymbalaria Fenzl in rats. Indian J Pharmacol 2007; 39(2): 90-6.
[http://dx.doi.org/10.4103/0253-7613.32527]
[62]
Shaik A, Kanhere RS, Cuddapah R, Nelson KS, Vara PR, Sibyala S. Antifertility activity of Artemisia vulgaris leaves on female Wistar rats. Chin J Nat Med 2014; 12(3): 180-5.
[http://dx.doi.org/10.1016/S1875-5364(14)60030-3] [PMID: 24702803]
[63]
Müller AL, Llados CM, Croxatto HB. Postcoital treatment with levonorgestrel does not disrupt postfertilization events in the rat. Contraception 2003; 67(5): 415-9.
[http://dx.doi.org/10.1016/S0010-7824(03)00021-0] [PMID: 12742567]
[64]
Liu T, Shi F, Ying Y, Chen Q, Tang Z, Lin H. Mouse model of menstruation: An indispensable tool to investigate the mechanisms of menstruation and gynaecological diseases. (Review). Mol Med Rep 2020; 22(6): 4463-74.
[http://dx.doi.org/10.3892/mmr.2020.11567] [PMID: 33174022]
[65]
Rina Aritonang T, Rahayu S, Irmawaty Sirait L, et al. The Role of FSH, LH, estradiol and progesterone hormone on estrus cycle of female rats. Int J Sci Basic Appl Res 2017; 35(1): 92-100.
[66]
Homburg R. Physiology of ovulation. In: Homburg R, Ed. Ovulation Induction and Controlled Ovarian Stimulation. 2nd ed. London, UK: Springer, Cham 2014; pp. 7-23.
[http://dx.doi.org/10.1007/978-3-319-05612-8_2]
[67]
Leyendecker G, Herbertz M, Kunz G, Mall G. Endometriosis results from the dislocation of basal endometrium. Hum Reprod 2002; 17(10): 2725-36.
[http://dx.doi.org/10.1093/humrep/17.10.2725] [PMID: 12351554]
[68]
Yamaguchi M, Yoshihara K, Suda K, et al. Three-dimensional understanding of the morphological complexity of the human uterine endometrium. iScience 2021; 24(4): 102258.
[http://dx.doi.org/10.1016/j.isci.2021.102258] [PMID: 33796844]
[69]
Raju GAR, Chavan R, Deenadayal M, et al. Luteinizing hormone and follicle stimulating hormone synergy: A review of role in controlled ovarian hyper-stimulation. J Hum Reprod Sci 2013; 6(4): 227-34.
[http://dx.doi.org/10.4103/0974-1208.126285] [PMID: 24672160]
[70]
Weiss G, Skurnick JH, Goldsmith LT, Santoro NF, Park SJ. Menopause and hypothalamic-pituitary sensitivity to estrogen. JAMA 2004; 292(24): 2991-6.
[http://dx.doi.org/10.1001/jama.292.24.2991] [PMID: 15613667]
[71]
Messinis IE. Ovarian feedback, mechanism of action and possible clinical implications. Hum Reprod Update 2006; 12(5): 557-71.
[http://dx.doi.org/10.1093/humupd/dml020] [PMID: 16672246]
[72]
Cervantes MP, Palomino JM, Adams GP. In vivo imaging in the rabbit as a model for the study of ovulation-inducing factors. Lab Anim 2015; 49(1): 1-9.
[http://dx.doi.org/10.1177/0023677214547406] [PMID: 25117585]
[73]
Ryu Y, Kim SW, Kim YY, Ku SY. Animal models for human polycystic ovary syndrome (PCOS) focused on the use of indirect hormonal perturbations: A review of the literature. Int J Mol Sci 2019; 20(11): 2720.
[http://dx.doi.org/10.3390/ijms20112720] [PMID: 31163591]
[74]
Shah M, Singh R, Shah R, Kakar S. An overview of the current methodologies used for evaluation of anti-fertility agents. Asian Pac J Reprod 2016; 5(3): 175-8.
[http://dx.doi.org/10.1016/j.apjr.2016.04.004]
[75]
Casarini L, Lispi M, Longobardi S, et al. LH and hCG action on the same receptor results in quantitatively and qualitatively different intracellular signalling. PLoS One 2012; 7(10): e46682.
[http://dx.doi.org/10.1371/journal.pone.0046682] [PMID: 23071612]
[76]
Liu Y, Li J, Zhang W, Guo Y. Association between serum oestradiol level on the hCG administration day and neonatal birthweight after IVF-ET among 3659 singleton live births. Sci Rep 2021; 11(1): 6084.
[http://dx.doi.org/10.1038/s41598-021-85692-7] [PMID: 33727635]
[77]
Demirel MA, Ilhan M, Suntar I, Keles H, Akkol EK. Activity of Corylus avellana seed oil in letrozole-induced polycystic ovary syndrome model in rats. Rev Bras Farmacogn 2016; 26(1): 83-8.
[http://dx.doi.org/10.1016/j.bjp.2015.09.009]
[78]
Choi J, Smitz J. Luteinizing hormone and human chorionic gonadotropin: Distinguishing unique physiologic roles. Gynecol Endocrinol 2014; 30(3): 174-81.
[http://dx.doi.org/10.3109/09513590.2013.859670] [PMID: 24283620]
[79]
Aquino NSS, Araujo-Lopes R, Henriques PC, et al. α-Estrogen and progesterone receptors modulate kisspeptin effects on prolactin: Role in estradiol-induced prolactin surge in female rats. Endocrinology 2017; 158(6): 1812-26.
[http://dx.doi.org/10.1210/en.2016-1855] [PMID: 28387824]
[80]
Papanikolaou EG, Kyrou D, Zervakakou G, Paggou E, Humaidan P. “Follicular HCG endometrium priming for IVF patients experiencing resisting thin endometrium. A proof of concept study”. J Assist Reprod Genet 2013; 30(10): 1341-5.
[http://dx.doi.org/10.1007/s10815-013-0076-0] [PMID: 23949214]
[81]
Bernardini L, Moretti-Rojas I, Brush M, Rojas FJ, Balmaceda JP. Failure of hCG/LH receptors to stimulate the transmembrane effector adenylyl cyclase in human endometrium. Adv Biosci Biotechnol 2013; 4(10): 949-57.
[http://dx.doi.org/10.4236/abb.2013.410126]
[82]
Gilbert SB, Roof AK, Rajendra Kumar T. Mouse models for the analysis of gonadotropin secretion and action. Best Pract Res Clin Endocrinol Metab 2018; 32(3): 219-39.
[http://dx.doi.org/10.1016/j.beem.2018.03.006] [PMID: 29779578]
[83]
Noh S, Go A, Kim D, Park M, Jeon HW, Kim B. Role of antioxidant natural products in management of infertility: A review of their medicinal potential. Antioxidants 2020; 9(10): 957.
[http://dx.doi.org/10.3390/antiox9100957]
[84]
Okafor IA, Nnamah US, Nnaka J. The fertility assessment of normal cyclic wistar rats following the administration of methanolic extract of Portulaca oleracea: An experimental study. Middle East Fertil Soc J 2021; 26(1): 5.
[http://dx.doi.org/10.1186/s43043-020-00048-x]
[85]
Ashkar F, Rezaei S, Salahshoornezhad S, et al. The Role of medicinal herbs in treatment of insulin resistance in patients with Polycystic Ovary Syndrome: A literature review. Biomol Concepts 2020; 11(1): 57-75.
[http://dx.doi.org/10.1515/bmc-2020-0005]
[86]
Abbara A, Vuong LN, Ho VNA, et al. Follicle size on day of trigger most likely to yield a mature oocyte. Front Endocrinol (Lausanne) 2018; 9: 193.
[http://dx.doi.org/10.3389/fendo.2018.00193] [PMID: 29743877]
[87]
Johnson R, Bennett WA, Cuadra EJ, Njiti V, Jung Y, Mason M. Roles of hCG in advancing follicular growth to ovulation after concurrent injections of PGF 2 and GnRH in postpubertal holstein heifers bearing a CL. Vet Med Int 2010; 2010: 394236.
[http://dx.doi.org/10.4061/2010/394236] [PMID: 21151654]
[88]
Hershko Klement A, Shulman A. hCG triggering in ART: An evolutionary concept. Int J Mol Sci 2017; 18(5): 1075.
[http://dx.doi.org/10.3390/ijms18051075] [PMID: 28513550]
[89]
Binelli M, Gonella-Diaza AM, Mesquita FS, Membrive CMB. Sex steroid-mediated control of oviductal function in cattle. Biology (Basel) 2018; 7(1): 15.
[http://dx.doi.org/10.3390/biology7010015] [PMID: 29393864]
[90]
Mokhtar DM. Microscopic and histochemical characterization of the bovine uterine tube during the follicular and luteal phases of estrous cycle. J Microsc Ultrastruct 2015; 3(1): 44-52.
[http://dx.doi.org/10.1016/j.jmau.2014.09.002] [PMID: 30023181]
[91]
Bu Z, Yang X, Song L, Kang B, Sun Y. The impact of endometrial thickness change after progesterone administration on pregnancy outcome in patients transferred with single frozen-thawed blastocyst. Reprod Biol Endocrinol 2019; 17(1): 99.
[http://dx.doi.org/10.1186/s12958-019-0545-0] [PMID: 31767010]
[92]
Andersson S, Minjarez D, Yost NP, Word RA. Estrogen and progesterone metabolism in the cervix during pregnancy and parturition. J Clin Endocrinol Metab 2008; 93(6): 2366-74.
[http://dx.doi.org/10.1210/jc.2007-2813] [PMID: 18364378]
[93]
Nakano FY, Leão R de BF, Esteves SC. Insights into the role of cervical mucus and vaginal pH in unexplained infertility. MedicalExpress (São Paulo) 2015; 2(2): 1-8.
[http://dx.doi.org/10.5935/MedicalExpress.2015.02.07]
[94]
Gaton E, Zejdel L, Bernstein D, Glezerman M, Czernobilsky B, Insler V. The effect of estrogen and gestagen on the mucus production of human endocervical cells: A histochemical study. Fertil Steril 1982; 38(5): 580-5.
[http://dx.doi.org/10.1016/S0015-0282(16)46638-0] [PMID: 6215266]
[95]
Dubey V, Tiwari RK, Mythirayee S, Gaharwar U, Pal M, Reddy S. Cervical mucus helps in the fertilization in women. World J Pharm Pharm Sci 2016; 5(10): 242-50.
[96]
Lee KY, DeMayo FJ. Animal models of implantation. Reproduction 2004; 128(6): 679-95.
[http://dx.doi.org/10.1530/rep.1.00340] [PMID: 15579585]
[97]
Guzeloglu-Kayisli O, Kayisli UA, Taylor HS. The role of growth factors and cytokines during implantation: Endocrine and paracrine interactions. Semin Reprod Med 2009; 27(1): 62-79.
[http://dx.doi.org/10.1055/s-0028-1108011] [PMID: 19197806]
[98]
Cui J, Shen Y, Li R. Estrogen synthesis and signaling pathways during aging: From periphery to brain. Trends Mol Med 2013; 19(3): 197-209.
[http://dx.doi.org/10.1016/j.molmed.2012.12.007] [PMID: 23348042]
[99]
Miro F, Parker SW, Aspinall LJ, Coley J, Perry PW, Ellis JE. Relationship between follicle-stimulating hormone levels at the beginning of the human menstrual cycle, length of the follicular phase and excreted estrogens: The FREEDOM study. J Clin Endocrinol Metab 2004; 89(7): 3270-5.
[http://dx.doi.org/10.1210/jc.2003-031732] [PMID: 15240602]
[100]
Rył A, Jasiewicz A, Grzywacz A, et al. Analysis of the relationship between estradiol and follicle-stimulating hormone concentrations and polymorphisms of apolipoprotein e and leptingenes in women post-menopause. Int J Environ Res Public Health 2016; 13(6): 543.
[http://dx.doi.org/10.3390/ijerph13060543] [PMID: 27240396]
[101]
Li C, Zhang HY, Liang Y, et al. Effects of Levonorgestrel and progesterone on Oviductal physiology in mammals. Reprod Biol Endocrinol 2018; 16(1): 59.
[http://dx.doi.org/10.1186/s12958-018-0377-3] [PMID: 29925391]
[102]
Kahlenborn C, Peck R, Severs WB. Mechanism of action of levonorgestrel emergency contraception. Linacre Q 2015; 82(1): 18-33.
[http://dx.doi.org/10.1179/2050854914Y.0000000026] [PMID: 25698840]
[103]
Zhao W, Zhu Q, Yan M, et al. Levonorgestrel decreases cilia beat frequency of human fallopian tubes and rat oviducts without changing morphological structure. Clin Exp Pharmacol Physiol 2015; 42(2): 171-8.
[http://dx.doi.org/10.1111/1440-1681.12337] [PMID: 25399777]
[104]
He W, Li X, Adekunbi D, et al. Hypothalamic effects of progesterone on regulation of the pulsatile and surge release of luteinising hormone in female rats. Sci Rep 2017; 7(1): 8096.
[http://dx.doi.org/10.1038/s41598-017-08805-1] [PMID: 28808344]
[105]
Khosravisamani M, Maliji G, Seyfi S, et al. Effect of the menstrual cycle on inflammatory cytokines in the periodontium. J Periodontal Res 2014; 49(6): 770-6.
[http://dx.doi.org/10.1111/jre.12161] [PMID: 24673464]
[106]
Devesa J, Almengló C, Devesa P. Multiple effects of growth hormone in the body: Is it really the hormone for growth? Clin Med Insights Endocrinol Diabetes 2016; 9: 47-71.
[http://dx.doi.org/10.4137/CMED.S38201] [PMID: 27773998]
[107]
Shivers KY, Amador N, Abrams L, Hunter D, Jenab S, Quiñones-Jenab V. Estrogen alters baseline and inflammatory-induced cytokine levels independent from hypothalamic-pituitary-adrenal axis activity. Cytokine 2015; 72(2): 121-9.
[http://dx.doi.org/10.1016/j.cyto.2015.01.007] [PMID: 25647266]
[108]
Dimitriadis E, White CA, Jones RL, Salamonsen LA. Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update 2005; 11(6): 613-30.
[http://dx.doi.org/10.1093/humupd/dmi023] [PMID: 16006437]
[109]
Idrees M, Oh SH, Muhammad T, El-Sheikh M, et al. Understanding the role of tyrosine phosphatase SHP2 in gametogenesis and early embryo development. Cell 2020; 1978.
[110]
Okumu LA, Forde N, Mamo S, et al. Temporal regulation of fibroblast growth factors and their receptors in the endometrium and conceptus during the pre-implantation period of pregnancy in cattle. Reproduction 2014; 147(6): 825-34.
[http://dx.doi.org/10.1530/REP-13-0373] [PMID: 24554351]
[111]
Singh M, Chaudhry P, Asselin E. Bridging endometrial receptivity and implantation: Network of hormones, cytokines, and growth factors. J Endocrinol 2011; 210(1): 5-14.
[http://dx.doi.org/10.1530/JOE-10-0461] [PMID: 21372150]
[112]
Islam MR, Yamagami K, Yoshii Y, Yamauchi N. Growth factor induced proliferation, migration, and lumen formation of rat endometrial epithelial cells in vitro. J Reprod Dev 2016; 62(3): 271-8.
[http://dx.doi.org/10.1262/jrd.2015-158] [PMID: 26946922]
[113]
Aflalo ED, Sod-Moriah UA, Potashnik G, Har-Vardi I. EGF increases expression and activity of PAs in preimplantation rat embryos and their implantation rate. Reprod Biol Endocrinol 2007; 5(1): 4.
[http://dx.doi.org/10.1186/1477-7827-5-4] [PMID: 17261179]
[114]
Paule S, Nebl T, Webb AI, Vollenhoven B, Rombauts LJ, Nie G. Proprotein convertase 5/6 cleaves platelet-derived growth factor A in the human endometrium in preparation for embryo implantation. Mol Hum Reprod 2015; 21(3): 262-70.
[http://dx.doi.org/10.1093/molehr/gau109] [PMID: 25429785]
[115]
Chatterjee P, Chiasson VL, Bounds KR, Mitchell BM. Regulation of the anti-inflammatory cytokines interleukin-4 and interleukin-10 during pregnancy. Front Immunol 2014; 5: 253.
[http://dx.doi.org/10.3389/fimmu.2014.00253] [PMID: 24904596]
[116]
Robertson SA, Care AS, Skinner RJ. Interleukin 10 regulates inflammatory cytokine synthesis to protect against lipopolysaccharide-induced abortion and fetal growth restriction in mice. Biol Reprod 2007; 76(5): 738-48.
[http://dx.doi.org/10.1095/biolreprod.106.056143] [PMID: 17215490]
[117]
Wang J, Huang C, Jiang R, et al. Decreased endometrial IL-10 impairs endometrial receptivity by downregulating HOXA10 expression in women with adenomyosis. BioMed Res Int 2018; 2018: 2549789.
[http://dx.doi.org/10.1155/2018/2549789] [PMID: 30687738]
[118]
Chen T, Darrasse-Jèze G, Bergot AS, et al. Self-specific memory regulatory T cells protect embryos at implantation in mice. J Immunol 2013; 191(5): 2273-81.
[http://dx.doi.org/10.4049/jimmunol.1202413] [PMID: 23913969]
[119]
Rosbottom A, Gibney EH, Guy CS, et al. Upregulation of cytokines is detected in the placentas of cattle infected with Neospora caninum and is more marked early in gestation when fetal death is observed. Infect Immun 2008; 76(6): 2352-61.
[http://dx.doi.org/10.1128/IAI.01780-06] [PMID: 18362132]
[120]
Jones TR, Ha J, Williams MA, et al. The role of the IL-2 pathway in costimulation blockade-resistant rejection of allografts. J Immunol 2002; 168(3): 1123-30.
[http://dx.doi.org/10.4049/jimmunol.168.3.1123] [PMID: 11801646]

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