The protective effects of Procyanidin C-1 on bisphenol a-induced testicular dysfunction in aged mice

Nieschlag, 2013, The conventional management of male infertility, Int. J. Gynecol. Obstet., 123, S31, 10.1016/j.ijgo.2013.09.001 Zegers-Hochschild, 2009, The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) Revised Glossary on ART Terminology, 2009, Hum. Reprod., 24, 2683, 10.1093/humrep/dep343 Brezina, 2012, Effects of pharmaceutical medications on male fertility, J. Reprod. Infertil, 13, 3 Plaseski, 2012, Association study of single-nucleotide polymorphisms in FASLG, JMJDIA, LOC203413, TEX15, BRDT, OR2W3, INSR, and TAS2R38 genes with male infertility, J. Androl., 33, 675, 10.2164/jandrol.111.013995 Chen, 2012, Low NRF2 mRNA expression in spermatozoa from men with low sperm motility, Tohoku, J. Exp. Med, 228, 259 Meyer, 2020, 509 Öztekin, 2020, The Relationship of male infertility with somatosensory amplification, health anxiety and depression levels, Psychiatry Investig, 17, 350, 10.30773/pi.2019.0248 Rato, 2019, 135 Perheentupa, 2019, Male infertility and environmental factors, Glob. Reprod. Heal., 4 Durairajanayagam, 2018, Lifestyle causes of male infertility, Arab J. Urol., 16, 10, 10.1016/j.aju.2017.12.004 Petersen, 2018, The effects of male age on sperm DNA damage: an evaluation of 2,178 semen samples, JBRA Assist. Reprod, 22, 323 Chianese, 2018, Chronic exposure to low dose of bisphenol A impacts on the first round of spermatogenesis via SIRT1 modulation, Sci. Rep., 8, 2961, 10.1038/s41598-018-21076-8 Siracusa, 2018, Effects of bisphenol A and its analogs on reproductive health: a mini review, Reprod. Toxic., 79, 96, 10.1016/j.reprotox.2018.06.005 Gonçalves, 2018, Bisphenol A reduces testosterone production in TM3 Leydig cells independently of its effects on cell death and mitochondrial membrane potential, Reprod. Toxicol., 76, 26, 10.1016/j.reprotox.2017.12.002 Peretz, 2014, Bisphenol A and reproductive health: update of experimental and human evidence, 2007-2013, Environ. Health Perspect., 122, 775, 10.1289/ehp.1307728 Martin, 2019, Births: final data for 2018, Natl. Vital Stat. Reports, 68, 1980 Khandwala, 2017, The age of fathers in the USA is rising: an analysis of 168 867 480 births from 1972 to 2015, Hum. Reprod, 32, 2110, 10.1093/humrep/dex267 Vaughan, 2020, DNA fragmentation of sperm: a radical examination of the contribution of oxidative stress and age in 16 945 semen samples, Hum. Reprod, 9 Mendoza-Wilson, 2016, Absorption of dimers, trimers and tetramers of procyanidins present in apple skin by IEC-18 cell monolayers, J. Funct. Foods, 27, 386, 10.1016/j.jff.2016.09.020 Zhao, 1999, Anti-tumor-promoting activity of a polyphenolic fraction isolated from grape seeds in the mouse skin two-stage initiation-promotion protocol and identification of procyanidin B5-3’-gallate as the most effective antioxidant constituent, Carcinogenesis, 20, 1737, 10.1093/carcin/20.9.1737 Cos, 2003, Comparative study of eight well-known polyphenolic antioxidants, J. Pharm. Pharmacol, 55, 1291, 10.1211/0022357021693 Kin, 2013, Procyanidin C1 from Cinnamomi Cortex inhibits TGF-β-induced epithelial-to-mesenchymal transition in the A549 lung cancer cell line, Int. J. Oncol., 43, 1901, 10.3892/ijo.2013.2139 Byun, 2012, A procyanidin trimer, C1, promotes NO production in rat aortic endothelial cells via both hyperpolarization and PI3K/Akt pathways, Eur. J. Pharmacol., 692, 52, 10.1016/j.ejphar.2012.07.011 Hori, 2015, Procyanidin trimer C1 derived from Theobroma cacao reactivates latent human immunodeficiency virus type 1 provirus, Biochem. Biophys. Res. Commun., 459, 288, 10.1016/j.bbrc.2015.02.102 Cary, 2018, Procyanidin trimer C1 reactivates latent HIV as a triple combination therapy with kansui and JQ1, PLoS One, 13, 1, 10.1371/journal.pone.0208055 Bae, 2020, Procyanidin C1 inhibits melanoma cell growth by activating 67-kDa laminin receptor signaling, Mol. Nutr. Food Res, 64, 1 Bahariv, 2016, The effects of phyllanthus gomphocarpus Hook. F. aqueous extract supplementation on androgenic hormonal level and histological testes morphometry, J. Teknol., 78, 55 Adler, 1996, Comparison of the duration of spermatogenesis between male rodents and humans, Mutat. Res., 352, 169, 10.1016/0027-5107(95)00223-5 June, 1992, Computer tracking of germ cells in the cycle of the seminiferous epithelium and prediction of changes in cycle duration in animals commonly used in reproductive biology and toxicology, J. Androl., 13, 185, 10.1002/j.1939-4640.1992.tb00297.x Festing, 2018, On determining sample size in experiments involving laboratory animals, Lab. Anim., 52, 341, 10.1177/0023677217738268 Arifin, 2017, Sample size calculation in animal studies using resource equation approach, Malaysian, J. Med. Sci, 24, 101 Chan, 2017, Anti-neuroinflammatory activity of Elephantopus scaber L. via activation of Nrf2/HO-1 signaling and inhibition of p38 MAPK pathway in LPS-induced microglia BV-2 cells, Front. Pharmacol., 8, 1, 10.3389/fphar.2017.00397 Hasanein, 2018, Ferulic acid prevents lead-induced testicular oxidative stress and suppressed spermatogenesis in rats, Andrologia, 50, 1, 10.1111/and.12798 Wang, 2019, Oral supplementation of fucoxanthin-rich brown algae extract ameliorates cisplatin-induced testicular damage in hamsters, Biomed. Pharmacother., 125 Nabavi, 2013, Effect of caffeine on motility and vitality of sperm and in vitro fertilization of outbreed mouse in T6 and M16 media, Iran, J. Reprod. Med., 11, 741 Binder, 2015, Male obesity is associated with changed spermatozoa Cox4i1 mRNA level and altered seminal vesicle fluid composition in a mouse model, Mol. Hum. Reprod., 21, 424, 10.1093/molehr/gav010 Dutta, 2013, Emblica officinalis Garten fruits extract ameliorates reproductive injury and oxidative testicular toxicity induced by chlorpyrifos in male rats, Springerplus, 2, 10.1186/2193-1801-2-541 Almabhouh, 2015, Effects of leptin on sperm count and morphology in Sprague-Dawley rats and their reversibility following a 6-week recovery period, Andrologia, 47, 751, 10.1111/and.12325 Behmanesh, 2018, Protective effect of aloe vera extract against bisphenol a induced testicular toxicity in wistar rats, Cell J, 20, 278 El Makawy, 2019, Effect of antiepileptic drug (Topiramate) and cold pressed ginger oil on testicular genes expression, sexual hormones and histopathological alterations in mice, Biomed. Pharmacother., 110, 409, 10.1016/j.biopha.2018.11.146 Zatecka, 2014, Effect of zearalenone on reproductive parameters and expression of selected testicular genes in mice, Reprod. Toxicol., 45, 20, 10.1016/j.reprotox.2014.01.003 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method, Methods, 25, 402, 10.1006/meth.2001.1262 Agarwal, 2015, A unique view on male infertility around the globe, Reprod. Biol. Endocrinol., 13, 37, 10.1186/s12958-015-0032-1 Srivastava, 2018, Alteration in apoptotic rate of testicular cells and sperms following administration of Bisphenol A (BPA) in Wistar albino rats, Environ. Sci. Pollut. Res., 25, 21635, 10.1007/s11356-018-2229-2 Cariati, 2019, Bisphenol a: an emerging threat to male fertility, Reprod. Biol. Endocrinol., 17, 6, 10.1186/s12958-018-0447-6 Marghani, 2018, Bisphenol a down-regulates the mrna expression of steroidogenic genes and induces histopathological changes in testes of rats, J. Vet. Healthc, 1, 32, 10.14302/issn.2575-1212.jvhc-18-2012 Ma, 2018, Lycopene reduces in utero bisphenol A exposure-induced mortality, benefits hormones, and development of reproductive organs in offspring mice, Environ. Sci. Pollut. Res., 25, 24041, 10.1007/s11356-018-2395-2 Mínguez-Alarcón, 2021, Paternal mixtures of urinary concentrations of phthalate metabolites, bisphenol A and parabens in relation to pregnancy outcomes among couples attending a fertility center, Environ. Int., 146, 10.1016/j.envint.2020.106171 Das, 2013, High prevalence of isolated sperm DNA damage in infertile men with advanced paternal age, J. Assist. Reprod. Genet., 30, 843, 10.1007/s10815-013-0015-0 Rosiak-Gill, 2019, Age-related changes in human sperm DNA integrity, Aging (Albany. NY), 11, 5399, 10.18632/aging.102120 Belloc, 2014, How to overcome male infertility after 40: influence of paternal age on fertility, Maturitas, 78, 22, 10.1016/j.maturitas.2014.02.011 Eisenberg, 2017, Effects of age on fertility and sexual function, Fertil. Steril., 107, 301, 10.1016/j.fertnstert.2016.12.018 Sharma, 2015, Effects of increased paternal age on sperm quality, reproductive outcome and associated epigenetic risks to offspring, Reprod. Biol. Endocrinol., 13, 35, 10.1186/s12958-015-0028-x du Fossé, 2020, Advanced paternal age is associated with an increased risk of spontaneous miscarriage: a systematic review and meta-analysis, Hum. Reprod. Update, 26, 650, 10.1093/humupd/dmaa010 Urhoj, 2017, Advanced paternal age and stillbirth rate: a nationwide register-based cohort study of 944,031 pregnancies in Denmark, Eur. J. Epidemiol., 32, 227, 10.1007/s10654-017-0237-z Shoji, 2006, Apple procyanidin oligomers absorption in rats after oral administration: analysis of procyanidins in plasma using the porter method and high-performance liquid chromatography/tandem mass spectrometry, J. Agric. Food Chem., 54, 884, 10.1021/jf052260b Wang, 2018, Absorption, metabolism, distribution and faecal excretion of B-type procyanidin oligomers in mice after a single oral administration of black soybean seed coat extract, Food Funct, 9, 5362, 10.1039/C8FO00852C Sun, 2019, Procyanidin C1, a Component of cinnamon extracts, is a potential insulin sensitizer that targets adipocytes, J. Agric. Food Chem., 67, 8839, 10.1021/acs.jafc.9b02932 Serra, 2010, Bioavailability of procyanidin dimers and trimers and matrix food effects in in vitro and in vivo models, Br. J. Nutr., 103, 944, 10.1017/S0007114509992741 Yamashita, 2016, Procyanidin promotes translocation of glucose transporter 4 in muscle of mice through activation of insulin and ampk signaling pathways, PLoS One, 11, 10.1371/journal.pone.0161704 Park, 2018, Protective effect of Lespedeza cuneata ethanol extract on Bisphenol A-induced testicular dysfunction in vivo and in vitro, Biomed. Pharmacother, 102, 76 Grami, 2020, Protective action of eruca sativa leaves aqueous extracts against bisphenol a-caused in vivo testicular damages, J. Med. Food, 23, 600, 10.1089/jmf.2019.0170 Zhang, 2013, Exposure to bisphenol A results in a decline in mouse spermatogenesis, Reprod. Fertil. Dev., 25, 847, 10.1071/RD12159 Kaur, 2018, Bisphenol A induced oxidative stress and apoptosis in mice testes: modulation by selenium, Andrologia, 50, 1, 10.1111/and.12834 Shin, 2017, Antioxidant and metalloproteinase inhibitory activities of ethanol extracts from Lespedeza cuneata G. Don, Korean J. Environ. Agric, 36, 263, 10.5338/KJEA.2017.36.4.40 Güleş, 2019, Protective effect of coenzyme Q10 against bisphenol-A-induced toxicity in the rat testes, Toxicol. Ind. Health, 35, 466, 10.1177/0748233719862475 Attia, 2010, Proanthocyanidins produce significant attenuation of doxorubicin-induced mutagenicity via suppression of oxidative stress, Oxid. Med. Cell. Longev., 3, 404, 10.4161/oxim.3.6.14418 Holdcraft, 2004, Hormonal regulation of spermatogenesis, Int. J. Androl., 27, 335, 10.1111/j.1365-2605.2004.00502.x Smith, 2014, The regulation of spermatogenesis by androgens, Semin. Cell Dev. Biol., 30, 2, 10.1016/j.semcdb.2014.02.012 Chimento, 2014, Role of estrogen receptors and G protein-coupled estrogen receptor in regulation of hypothalamus-pituitary-testis axis and spermatogenesis, Front. Endocrinol. (Lausanne)., 5, 1, 10.3389/fendo.2014.00001 Brouard, 2016, Differential effects of bisphenol A and estradiol on rat spermatogenesis’ establishment, Reprod. Toxicol., 63, 49, 10.1016/j.reprotox.2016.05.003 Zang, 2016, Effects of bisphenol a on testosterone levels and sexual behaviors of male mice, Adv. Sex. Med, 6, 41, 10.4236/asm.2016.64006 Olukole, 2018, Melatonin ameliorates bisphenol A-induced perturbations of the prostate gland of adult Wistar rats, Biomed. Pharmacother., 105, 73, 10.1016/j.biopha.2018.05.125 Hasona, 2018, Grape seed extract attenuates dexamethasone-induced testicular and thyroid dysfunction in male albino rats, Andrologia, 50, 1, 10.1111/and.13002 Sjöström, 2002, The predictive value of bcl-2, bax, bcl-xL, bag-1, fas, and fasL for chemotherapy response in advanced breast cancer, Clin. Cancer Res., 8, 811 Wang, 2014, Mitochondrion-mediated apoptosis is involved in reproductive damage caused by BPA in male rats, Environ. Toxicol. Pharmacol., 38, 1025, 10.1016/j.etap.2014.10.018 Ok, 2017, Cultivated wild ginseng extracts upregulate the anti-apoptosis systems in cells and mice induced by bisphenol A, Mol. Cell. Toxicol., 13, 73, 10.1007/s13273-017-0008-7 Meyer, 2017, Mitochondrial fusion, fission, and mitochondrial toxicity, Toxicology, 391, 42, 10.1016/j.tox.2017.07.019 Amanpour, 2020, Protective effects of vitamin E on cadmium-induced apoptosis in rat testes, Naunyn. Schmiedebergs. Arch. Pharmacol., 393, 349, 10.1007/s00210-019-01736-w