Prenatal exposure to acrylamide differently affected the sex ratio, aromatase and apoptosis in female adult offspring of two subsequent generations
Jazyk angličtina Země Česko Médium print-electronic
Typ dokumentu časopisecké články
PubMed
36545876
PubMed Central
PMC10069810
DOI
10.33549/physiolres.934975
PII: 934975
Knihovny.cz E-zdroje
- MeSH
- akrylamid toxicita MeSH
- apoptóza MeSH
- aromatasa * genetika MeSH
- furylfuramid MeSH
- krysa rodu Rattus MeSH
- lidé MeSH
- poměr pohlaví MeSH
- potkani Wistar MeSH
- těhotenství MeSH
- zpožděný efekt prenatální expozice * chemicky indukované MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- lidé MeSH
- těhotenství MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- akrylamid MeSH
- aromatasa * MeSH
- furylfuramid MeSH
In the present study, we investigated the effect of acrylamide (ACR) exposure during pregnancy on the ovary of female adult offspring of two subsequent generations. Sixty-day-old Wistar albino female rats were given different doses of ACR (2.5 and 10 mg/kg/day) from day 6 of pregnancy until giving birth. Females from the first generation (AF1) were fed ad libitum, and thereafter, a subgroup was euthanized at 8 weeks of age and ovary samples were obtained. The remaining females were maintained until they reached sexual maturity (50 days old) and then treated in the same way as the previous generation to obtain the second generation of females (AF2). The histopathological examination indicated a high frequency of corpora lutea along with an increased number of antral follicles that reached the selectable stage mainly at a dose of 2.5 mg/kg/day. Interestingly, ACR exposure significantly increased the mRNA levels of CYP19 gene and its corresponding CYP19 protein expression in AF1 females. The TUNEL assay showed a significantly high rate of apoptosis in stromal cells except for dose of 2.5 mg/kg/day. However, in AF2 females, ACR exposure significantly increased the number of degenerating follicles and cysts while the number of growing follicles was reduced. Moreover, in both ACR-treated groups, estradiol-producing enzyme CYP19A gene and its corresponding protein were significantly reduced, and an excessive apoptosis was produced. We concluded that the ovarian condition of AF1 females had considerable similarity to the typical early perimenopausal stage, whereas that of AF2 females was similar to the late perimenopausal stage in women.
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Silvestris E, Lovero D, Palmirotta R. Nutrition and female fertility: an interdependent correlation. Fron Endocrinol (Lausanne) 2019;10:346. doi: 10.3389/fendo.2019.00346. PubMed DOI PMC
Hanson B, Johnstone E, Dorais J, Silver B, Peterson CM, Hotaling J. Female infertility, infertility-associated diagnoses, and comorbidities: a review. J Assist Reprod Genet. 2017;34:167–177. doi: 10.1007/s10815-016-0836-8. PubMed DOI PMC
Jalouli M, Mofti A, Elnakady YA, Nahdi S, Feriani A, Alrezaki A, Sebei K, et al. Allethrin promotes apoptosis and autophagy associated with the oxidative stress-related PI3K/AKT/mTOR signaling pathway in developing rat ovaries. Int J Mol Sci. 2022;23:6397. doi: 10.3390/ijms23126397. PubMed DOI PMC
Tarko A, Štochmal’ová A, Hrabovszká S, Vachanová A, Harrath AH, Aldahmash W, Grossman R, Sirotkin AV. Potential protective effect of puncture vine (Tribulus terrestris, L.) against xylene toxicity on bovine ovarian cell functions. Physiol Res. 2022;71:249. doi: 10.33549/physiolres.934871. PubMed DOI PMC
Harrath AH, Alrezaki A, Mansour L, Alwasel SH, Palomba S. Food restriction during pregnancy and female offspring fertility: adverse effects of reprogrammed reproductive lifespan. J Ovarian Res. 2017;10:1–9. doi: 10.1186/s13048-017-0372-x. PubMed DOI PMC
Harrath AH, Alrezaki A, Jalouli M, Al-Dawood N, Dahmash W, Mansour L, Sirotkin A, Alwasel S. Benzene exposure causes structural and functional damage in rat ovaries: occurrence of apoptosis and autophagy. Environ Sci Pollut Res Int. 2022;29:76275–76285. doi: 10.1007/s11356-022-21289-5. PubMed DOI
Harrath AH, Alrezaki A, Jalouli M, Aldawood N, Aldahmash W, Mansour L, Alwasel S. Ethylbenzene exposure disrupts ovarian function in Wistar rats via altering folliculogenesis and steroidogenesis-related markers and activating autophagy and apoptosis. Ecotoxicol Environ Saf. 2022;229:113081. doi: 10.1016/j.ecoenv.2021.113081. PubMed DOI
Sirotkin AV, Dekanová P, Harrath AH. FSH, oxytocin and IGF-I regulate the expression of sirtuin 1 in porcine ovarian granulosa cells. Physiol Res. 2020;69:461. doi: 10.33549/physiolres.934424. PubMed DOI PMC
Practice Committee of the American Society for Reproductive M. Smoking and infertility. Fertil Steril. 2004;81:1181–1186. doi: 10.1016/j.fertnstert.2003.11.024. PubMed DOI
Higgins S. Smoking in pregnancy. Curr Opin Obstet Gynecol. 2002;14:145–151. doi: 10.1097/00001703-200204000-00007. PubMed DOI
Wetendorf M, Randall LT, Lemma MT, Hurr SH, Pawlak JB, Tarran R, Doerschuk CM, Caron KM. E-cigarette exposure delays implantation and causes reduced weight gain in female offspring exposed in utero. J Endocr Soc. 2019;3:1907–1916. doi: 10.1210/js.2019-00216. PubMed DOI PMC
Rodriguez HA, Santambrosio N, Santamaria CG, Munoz-de-Toro M, Luque EH. Neonatal exposure to bisphenol A reduces the pool of primordial follicles in the rat ovary. Reprod Toxicol. 2010;30:550–557. doi: 10.1016/j.reprotox.2010.07.008. PubMed DOI
Ozel S, Tokmak A, Aykut O, Aktulay A, Hancerliogullari N, Engin Ustun Y. Serum levels of phthalates and bisphenol-A in patients with primary ovarian insufficiency. Gynecol Endocrinol. 2019;35:364–367. doi: 10.1080/09513590.2018.1534951. PubMed DOI
Friedman M. Chemistry, biochemistry, and safety of acrylamide. A review. J Agric Food Chem. 2003;51:4504–4526. doi: 10.1021/jf030204. PubMed DOI
Aldawood N, Alrezaki A, Alanazi S, Amor N, Alwasel S, Sirotkin A, Harrath AH. Acrylamide impairs ovarian function by promoting apoptosis and affecting reproductive hormone release, steroidogenesis and autophagy-related genes: An in vivo study. Ecotoxicol Environ Saf. 2020;197:110595. doi: 10.1016/j.ecoenv.2020.110595. PubMed DOI
Tilson HA. The neurotoxicity of acrylamide: an overview. Neurobehav Toxicol Teratol. 1981;3:445–461. PubMed
Smith EA, Oehme FW. Acrylamide and polyacrylamide: a review of production, use, environmental fate and neurotoxicity. Rev Environ Health. 1991;9:215–228. doi: 10.1515/REVEH.1991.9.4.215. PubMed DOI
Adler ID, Gonda H, Hrabe de Angelis M, Jentsch I, Otten IS, Speicher MR. Heritable translocations induced by dermal exposure of male mice to acrylamide. Cytogenet Genome Res. 2004;104:271–276. doi: 10.1159/000077501. PubMed DOI
Żyzelewicz D, Nebesny E, Oracz J. Acrylamide - formation, physicochemical and biological properties. (Article in Polish) Bromat Chem Toksykol. 2010;3:415–427.
Szczerbina T. Acrylamide as probable carcinogen in food. (Article in Polish) Kosmos. 2005;54:367–372.
Moldoveanu SC, Gerardi AR. Acrylamide analysis in tobacco, alternative tobacco products, and cigarette smoke. J Chromatogr Sci. 2011;49:234–242. doi: 10.1093/chrsci/49.3.234. DOI
Carere A. Genotoxicity and carcinogenicity of acrylamide: a critical review. Ann Ist Super Sanita. 2006;42:144–155. PubMed
Vesper HW, Bernert JT, Ospina M, Meyers T, Ingham L, Smith A, Myers GL. Assessment of the relation between biomarkers for smoking and biomarkers for acrylamide exposure in humans. Cancer Epidemiol Biomarkers Prev. 2007;16:2471–2478. doi: 10.1158/1055-9965.EPI-06-1058. PubMed DOI
Hogervorst JG, Schouten LJ, Konings EJ, Goldbohm RA, van den Brandt PA. Dietary acrylamide intake and the risk of renal cell, bladder, and prostate cancer. Am J Clin Nutr. 2008;87:1428–1438. doi: 10.1093/ajcn/87.5.1428. PubMed DOI
Tareke E, Rydberg P, Karlsson P, Eriksson S, Tornqvist M. Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J Agric Food Chem. 2002;50:4998–5006. doi: 10.1021/jf020302f. PubMed DOI
Becalski A, Lau BP, Lewis D, Seaman SW. Acrylamide in foods: occurrence, sources, and modeling. J Agric Food Chem. 2003;51:802–808. doi: 10.1021/jf020889y. PubMed DOI
EFSA. Results on the monitoring of acrylamide levels in food. EFSA Scientific Report. EFSA J. 2009;7:2–26. doi: 10.2903/j.efsa.2009.285r. DOI
Mojska H, Gielecińska I. Assessment of exposure of children and youth to acrylamide in fast foods and snacks. Probl Hig Epidemiol. 2012;93:613–617.
Aldawood N, Alrezaki A, Alanazi S, Amor N, Alwasel S, Sirotkin A, Harrath AH. Acrylamide impairs ovarian function by promoting apoptosis and affecting reproductive hormone release, steroidogenesis and autophagy-related genes: An in vivo study. Ecotoxicol Environ Saf. 2020;197:110595. doi: 10.1016/j.ecoenv.2020.110595. PubMed DOI
Lai SM, Gu ZT, Zhao MM, Li XX, Ma YX, Luo L, Liu J. Toxic effect of acrylamide on the development of hippocampal neurons of weaning rats. Neural Regen Res. 2017;12:1648–1654. doi: 10.4103/1673-5374.217345. PubMed DOI PMC
Zhang Y, Huang M, Zhuang P, Jiao J, Chen X, Wang J, Wu Y. Exposure to acrylamide and the risk of cardiovascular diseases in the National Health and Nutrition Examination Survey 2003–2006. Environ Int. 2018;117:154–163. doi: 10.1016/j.envint.2018.04.047. PubMed DOI
Allam AA, El-Ghareeb AW, Abdul-Hamid M, Bakery AE, Gad M, Sabri M. Effect of prenatal and perinatal acrylamide on the biochemical and morphological changes in liver of developing albino rat. Arch Toxicol. 2010;84:129–141. doi: 10.1007/s00204-009-0475-2. PubMed DOI
Nagata C, Konishi K, Tamura T, Wada K, Tsuji M, Hayashi M, Takeda N, Yasuda K. Associations of acrylamide intake with circulating levels of sex hormones and prolactin in premenopausal Japanese women. Cancer Epidemiol Biomarkers Prev. 2015;24:249–254. doi: 10.1158/1055-9965.EPI-14-0935. PubMed DOI
Hogervorst JG, Fortner RT, Mucci LA, Tworoger SS, Eliassen AH, Hankinson SE, Wilson KM. Associations between dietary acrylamide intake and plasma sex hormone levels. Cancer Epidemiol Biomarkers Prev. 2013;22:2024–2036. doi: 10.1158/1055-9965.EPI-13-0509. PubMed DOI PMC
Nagahama Y, Chakraborty T, Paul-Prasanth B, Ohta K, Nakamura M. Sex determination, gonadal sex differentiation, and plasticity in vertebrate species. Physiol Rev. 2021;101:1237–1308. doi: 10.1152/physrev.00044.2019. PubMed DOI
Capel B. Vertebrate sex determination: evolutionary plasticity of a fundamental switch. Nat Rev Genet. 2017;18:675–689. doi: 10.1038/nrg.2017.60. PubMed DOI
Shao C, Li Q, Chen S, Zhang P, Lian J, Hu Q, Sun B, Jin L, Liu S, Wang Z. Epigenetic modification and inheritance in sexual reversal of fish. Genome Res. 2014;24:604–615. doi: 10.1101/gr.162172.113. PubMed DOI PMC
Prior JC. Perimenopause: the complex endocrinology of the menopausal transition. Endocr Rev. 1998;19:397–428. doi: 10.1210/edrv.19.4.0341. PubMed DOI
Prior JC. Ovarian aging and the perimenopausal transition: the paradox of endogenous ovarian hyperstimulation. Endocrine. 2005;26:297–300. doi: 10.1385/ENDO:26:3:297. PubMed DOI
te Velde ER, Scheffer GJ, Dorland M, Broekmans FJ, Fauser BC. Developmental and endocrine aspects of normal ovarian aging. Mol Cell Endocrinol. 1998;145:67–73. doi: 10.1016/S0303-7207(98)00171-3. PubMed DOI
Shaw ND, Srouji SS, Welt CK, Cox KH, Fox JH, Adams JA, Sluss PM, Hall JE. Compensatory increase in ovarian aromatase in older regularly cycling women. J Clin Endocrinol Metab. 2015;100:3539–3547. doi: 10.1210/JC.2015-2191. PubMed DOI PMC
Klein NA, Battaglia DE, Fujimoto VY, Davis GS, Bremner WJ, Soules MR. Reproductive aging: accelerated ovarian follicular development associated with a monotropic follicle-stimulating hormone rise in normal older women. J Clin Endocrinol Metab. 1996;81:1038–1045. doi: 10.1210/jcem.81.3.8772573. PubMed DOI
Nicosia S. The aging ovary. Med Clin North Am. 1987;71:1–9. doi: 10.1016/S0025-7125(16)30878-1. PubMed DOI
Beckers NG, Macklon NS, Eijkemans MJ, Fauser BC. Women with regular menstrual cycles and a poor response to ovarian hyperstimulation for in vitro fertilization exhibit follicular phase characteristics suggestive of ovarian aging. Fertil Steril. 2002;78:291–297. doi: 10.1016/S0015-0282(02)03227-2. PubMed DOI
Hamdine O, Macklon NS, Eijkemans MJ, Laven JS, Cohlen BJ, Verhoeff A, van Dop PA, et al. Elevated early follicular progesterone levels and in vitro fertilization outcomes: a prospective intervention study and meta-analysis. Fertil Steril. 2014;102:448–454.e1. doi: 10.1016/j.fertnstert.2014.05.002. PubMed DOI
Umehara T, Richards JS, Shimada M. The stromal fibrosis in aging ovary. Aging (Albany NY) 2018;10:9–10. doi: 10.18632/aging.101370. PubMed DOI PMC
Abdollahifar MA, Azad N, Sajadi E, Shams Mofarahe Z, Zare F, Moradi A, Rezaee F, Gholamin M, Abdi S. Vitamin C restores ovarian follicular reservation in a mouse model of aging. Anat Cell Biol. 2019;52:196–203. doi: 10.5115/acb.2019.52.2.196. PubMed DOI PMC
Welt CK. Primary ovarian insufficiency: a more accurate term for premature ovarian failure. Clin Endocrinol (Oxf) 2008;68:499–509. doi: 10.1111/j.1365-2265.2007.03073.x. PubMed DOI
Cordts EB, Christofolini DM, Dos Santos AA, Bianco B, Barbosa CP. Genetic aspects of premature ovarian failure: a literature review. Arch Gynecol Obstet. 2011;283:635–643. doi: 10.1007/s00404-010-1815-4. PubMed DOI
Endogenous Hormones and Breast Cancer Collaborative Group. Key TJ, Appleby PN, Reeves GK, Travis RC, Alberg AJ, Barricarte A, et al. Sex hormones and risk of breast cancer in premenopausal women: a collaborative reanalysis of individual participant data from seven prospective studies. Lancet Oncol. 2013;14:1009–1019. doi: 10.1016/S1470-2045(13)70301-2. PubMed DOI PMC
Olesen PT, Olsen A, Frandsen H, Frederiksen K, Overvad K, Tjonneland A. Acrylamide exposure and incidence of breast cancer among postmenopausal women in the Danish Diet, Cancer and Health Study. Int J Cancer. 2008;122:2094–2100. doi: 10.1002/ijc.23359. PubMed DOI
Klinger FG, Rossi V, De Felici M. Multifaceted programmed cell death in the mammalian fetal ovary. Int J Dev Biol. 2015;59:51–54. doi: 10.1387/ijdb.150063fk. PubMed DOI
Marder W, Fisseha S, Ganser MA, Somers EC. Ovarian damage during chemotherapy in autoimmune diseases: broad health implications beyond fertility. Clin Med Insights Reprod Health. 2012;2012:9–18. doi: 10.4137/CMRH.S10415. PubMed DOI PMC
Folsom LJ, Fuqua JS. reproductive issues in women with Turner syndrome. Endocrinol Metab Clin North Am. 2015;44:723–737. doi: 10.1016/j.ecl.2015.07.004. PubMed DOI PMC
Yu K, Zhang X, Tan X, Ji M, Chen Y, Tao Y, Liu M, Yu Z. Transgenerational impairment of ovarian induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) associated with Igf2 and H19 in adult female rat. Toxicology. 2019;428:152311. doi: 10.1016/j.tox.2019.152311. PubMed DOI
Thomford PJ, Jelovsek FR, Mattison DR. Effect of oocyte number and rate of atresia on the age of menopause. Reprod Toxicol. 1987;1:41–51. doi: 10.1016/0890-6238(87)90070-0. PubMed DOI
Abbott DH, Dumesic DA, Eisner JR, Colman RJ, Kemnitz JW. Insights into the development of polycystic ovary syndrome (PCOS) from studies of prenatally androgenized female rhesus monkeys. Trends Endocrinol Metab. 1998;9:62–67. doi: 10.1016/S1043-2760(98)00019-8. PubMed DOI
Kezele P, Skinner MK. Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: endocrine model of follicle assembly. Endocrinology. 2003;144:3329–3337. doi: 10.1210/en.2002-0131. PubMed DOI
Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology. 2007;148:3580–3590. doi: 10.1210/en.2007-0088. PubMed DOI
Haney AF, Newbold RR, McLachlan JA. Prenatal diethylstilbestrol exposure in the mouse: effects on ovarian histology and steroidogenesis in vitro. Biol Reprod. 1984;30:471–478. doi: 10.1095/biolreprod30.2.471. PubMed DOI
Broekmans FJ, Soules MR, Fauser BC. Ovarian aging: mechanisms and clinical consequences. Endocr Rev. 2009;30:465–493. doi: 10.1210/er.2009-0006. PubMed DOI
Nelson SM, Telfer EE, Anderson RA. The ageing ovary and uterus: new biological insights. Hum Reprod Update. 2013;19:67–83. doi: 10.1093/humupd/dms043. PubMed DOI PMC