Association between heat stress during intrauterine development and the expression and regulation of ovarian steroid hormone receptors in adult Holstein cows
Fernanda M. Rodríguez A B # , Ulises S. Notaro A # , Emilia Huber A , Sebastián Recce B , Hugo H. Ortega A B , Marcelo L. Signorini B C , Florencia Rey
A B and Natalia R. Salvetti A B *
+ Author Affiliations
- Author Affiliations
A Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Esperanza, Santa Fe, Argentina.
B Facultad de Ciencias Veterinarias del Litoral, UNL, Esperanza, Santa Fe, Argentina.
C Instituto Nacional de Tecnología Agropecuaria (INTA) EEA Rafaela, Santa Fe, Argentina.
* Correspondence to: salvetti@fcv.unl.edu.ar
# These authors contributed equally to this paper
Handling Editor: Jennifer Juengel
Reproduction, Fertility and Development 34(16) 1003-1022 https://doi.org/10.1071/RD22067
Published online: 16 September 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Dairy cattle experience stressful environmental situations that affect production. Heat stress during gestation can influence the intrauterine development of offspring, resulting in long-term damage that can affect the reproductive life of the adult offspring.
Aim: The aim of the present study was to evaluate changes in the expression and regulation of steroid hormone receptors in the ovary of Holstein cows gestated under different temperature-humidity index (THI) during their in utero development.
Methods: Animals were classified by their exposure to temperature-humidity index (THI) ≥72 during their development in utero according to date of birth or date of effective service of their mother. This study was not carried out under controlled conditions, but the conditions to which the cows were naturally exposed during their development were considered retrospectively, controlling the variables in the statistical analyses (age as a covariate, dairy farm as a random factor). Gestation was divided into two periods (P1 = days 0–150; and P2 = day 151 to calving) and three trimesters (T1 = days 0–90; T2 = days 91–180; and T3 = day 181 to calving), and the exposure to THI ≥72 was calculated in each one. The following characteristics were evaluated: gene expression of estrogen receptor (ESR) 1, ESR2 and progesterone receptor (PGR), CpG methylation in the 5′UTR of ESR1 and ESR2, and protein expression of ESR1, ESR2, PGR and coregulatory proteins in the dominant follicles of daughter cows in adulthood.
Key results: We found associations between heat stress variables during gestation and the methylation status of CpG sites in the 5′UTR of ESR1 and ESR2 in dominant follicles. Results also showed association between exposure to high THI values during intrauterine development and expression of ESR1, ESR2 and PGR and coregulatory proteins in dominant follicles of adult cows.
Conclusions: These results provide novel information about the impact of prenatal heat stress on molecular aspects at the ovary level in the offspring, during their adult life, which probably impacts the reproductive aspects of the herd.
Keywords: cattle, coregulatory proteins, epigenetics, heat stress, intrauterine development, offspring, ovary, steroid receptors.
References
Abedel-Majed, MA, Romereim, SM, Davis, JS, and Cupp, AS (2019). Perturbations in lineage specification of granulosa and theca cells may alter corpus luteum formation and function. Frontiers in Endocrinology 10, 832.| Perturbations in lineage specification of granulosa and theca cells may alter corpus luteum formation and function.Crossref | GoogleScholarGoogle Scholar |
Abruzzese, GA, Crisosto, N, De Grava Kempinas, W, and Sotomayor-Zárate, R (2018). Developmental programming of the female neuroendocrine system by steroids. Journal of Neuroendocrinology 30, e12632.
| Developmental programming of the female neuroendocrine system by steroids.Crossref | GoogleScholarGoogle Scholar |
Ahmed, BMS, Younas, U, Asar, TO, Dikmen, S, Hansen, PJ, and Dahl, GE (2017). Cows exposed to heat stress during fetal life exhibit improved thermal tolerance. Journal of Animal Science 95, 3497–3503.
| Cows exposed to heat stress during fetal life exhibit improved thermal tolerance.Crossref | GoogleScholarGoogle Scholar |
Akbarinejad, V, Gharagozlou, F, and Vojgani, M (2017). Temporal effect of maternal heat stress during gestation on the fertility and anti-Müllerian hormone concentration of offspring in bovine. Theriogenology 99, 69–78.
| Temporal effect of maternal heat stress during gestation on the fertility and anti-Müllerian hormone concentration of offspring in bovine.Crossref | GoogleScholarGoogle Scholar |
Alfaro, NS, Salvetti, NR, Velazquez, MM, Stangaferro, ML, Rey, F, and Ortega, HH (2012). Steroid receptor mRNA expression in the ovarian follicles of cows with cystic ovarian disease. Research in Veterinary Science 92, 478–485.
| Steroid receptor mRNA expression in the ovarian follicles of cows with cystic ovarian disease.Crossref | GoogleScholarGoogle Scholar |
Allen, JJ, Herrick, SL, and Fortune, JE (2016). Regulation of steroidogenesis in fetal bovine ovaries: differential effects of LH and FSH. Journal of Molecular Endocrinology 57, 275–286.
| Regulation of steroidogenesis in fetal bovine ovaries: differential effects of LH and FSH.Crossref | GoogleScholarGoogle Scholar |
Apostolakis, EM, Ramamurphy, M, Zhou, D, Oñate, S, and O’Malley, BW (2002). Acute disruption of select steroid receptor coactivators prevents reproductive behavior in rats and unmasks genetic adaptation in knockout mice. Molecular Endocrinology 16, 1511–1523.
| Acute disruption of select steroid receptor coactivators prevents reproductive behavior in rats and unmasks genetic adaptation in knockout mice.Crossref | GoogleScholarGoogle Scholar |
Auger, AP, and Jessen, HM (2009). Corepressors, nuclear receptors, and epigenetic factors on DNA: a tail of repression. Psychoneuroendocrinology 34, S39–S47.
| Corepressors, nuclear receptors, and epigenetic factors on DNA: a tail of repression.Crossref | GoogleScholarGoogle Scholar |
Baddela, VS, Baufeld, A, Yenuganti, VR, Vanselow, J, and Singh, D (2014). Suitable housekeeping genes for normalization of transcript abundance analysis by real-time RT-PCR in cultured bovine granulosa cells during hypoxia and differential cell plating density. Reproductive Biology and Endocrinology 12, 118.
| Suitable housekeeping genes for normalization of transcript abundance analysis by real-time RT-PCR in cultured bovine granulosa cells during hypoxia and differential cell plating density.Crossref | GoogleScholarGoogle Scholar |
Bar-Sadeh, B, Rudnizky, S, Pnueli, L, Bentley, GR, Stöger, R, Kaplan, A, and Melamed, P (2020). Unravelling the role of epigenetics in reproductive adaptations to early-life environment. Nature Reviews Endocrinology 16, 519–533.
| Unravelling the role of epigenetics in reproductive adaptations to early-life environment.Crossref | GoogleScholarGoogle Scholar |
Bello, NM, Steibel, JP, and Pursley, JR (2006). Optimizing ovulation to first GnRH improved outcomes to each hormonal injection of ovsynch in lactating dairy cows. Journal of Dairy Science 89, 3413–3424.
| Optimizing ovulation to first GnRH improved outcomes to each hormonal injection of ovsynch in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |
Belotti, EM, Stassi, AF, Velázquez, MML, Díaz, PU, Marelli, BE, Rey, F, Notaro, US, Ortega, HH, and Salvetti, NR (2017). Changes in the proliferation/apoptosis balance in the bovine ovary: a key early event in follicular persistence. Cells Tissues Organs 204, 314–325.
| Changes in the proliferation/apoptosis balance in the bovine ovary: a key early event in follicular persistence.Crossref | GoogleScholarGoogle Scholar |
Belotti, EM, Amweg, AN, Matiller, V, Varela, ML, Stassi, AF, Velázquez, MML, Ortega, HH, Rey, F, and Salvetti, NR (2020). Effects of adrenocorticotrophic hormone on the expression of matrix metalloproteinases and their inhibitors in the bovine ovary. Reproduction, Fertility and Development 32, 748–762.
| Effects of adrenocorticotrophic hormone on the expression of matrix metalloproteinases and their inhibitors in the bovine ovary.Crossref | GoogleScholarGoogle Scholar |
Binelli, M, and Murphy, BD (2010). Coordinated regulation of follicle development by germ and somatic cells. Reproduction, Fertility and Development 22, 1–12.
| Coordinated regulation of follicle development by germ and somatic cells.Crossref | GoogleScholarGoogle Scholar |
Bramley, T (2003). Non-genomic progesterone receptors in the mammalian ovary: some unresolved issues. Reproduction 125, 3–15.
| Non-genomic progesterone receptors in the mammalian ovary: some unresolved issues.Crossref | GoogleScholarGoogle Scholar |
Braw-Tal, R, and Yossefi, S (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. Journal of Reproduction and Fertility 109, 165–171.
| Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary.Crossref | GoogleScholarGoogle Scholar |
Burkhart, MN, Juengel, JL, Smith, PR, Heath, DA, Perry, GA, Smith, MF, and Garverick, HA (2010). Morphological development and characterization of aromatase and estrogen receptors alpha and beta in fetal ovaries of cattle from days 110 to 250. Animal Reproduction Science 117, 43–54.
| Morphological development and characterization of aromatase and estrogen receptors alpha and beta in fetal ovaries of cattle from days 110 to 250.Crossref | GoogleScholarGoogle Scholar |
Bustin, SA, Benes, V, Garson, JA, Hellemans, J, Huggett, J, Kubista, M, Mueller, R, Nolan, T, Pfaffl, MW, Shipley, GL, Vandesompele, J, and Wittwer, CT (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.
| The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar |
Calder, MD, Manikkam, M, Salfen, BE, Youngquist, RS, Lubahn, DB, Lamberson, WR, and Garverick, HA (2001). Dominant bovine ovarian follicular cysts express increased levels of messenger RNAs for luteinizing hormone receptor and 3β-hydroxysteroid dehydrogenase Δ4, Δ5 isomerase compared to normal dominant follicles. Biology of Reproduction 476, 471–476.
| Dominant bovine ovarian follicular cysts express increased levels of messenger RNAs for luteinizing hormone receptor and 3β-hydroxysteroid dehydrogenase Δ4, Δ5 isomerase compared to normal dominant follicles.Crossref | GoogleScholarGoogle Scholar |
Coolen, MW, Statham, AL, Gardiner-Garden, M, and Clark, SJ (2007). Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Research 35, e119.
| Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements.Crossref | GoogleScholarGoogle Scholar |
Dahl, GE, Skibiel, AL, and Laporta, J (2019). In utero heat stress programs reduced performance and health in calves. Veterinary Clinics of North America: Food Animal Practice 35, 343–353.
| In utero heat stress programs reduced performance and health in calves.Crossref | GoogleScholarGoogle Scholar |
Deaton, AM, and Bird, A (2011). CpG islands and the regulation of transcription. Genes & Development 25, 1010–1022.
| CpG islands and the regulation of transcription.Crossref | GoogleScholarGoogle Scholar |
Díaz, PU, Stangaferro, ML, Gareis, NC, Silvia, WJ, Matiller, V, Salvetti, NR, Rey, F, Barberis, F, Cattaneo, L, and Ortega, HH (2015). Characterization of persistent follicles induced by prolonged treatment with progesterone in dairy cows: an experimental model for the study of ovarian follicular cysts. Theriogenology 84, 1149–1160.
| Characterization of persistent follicles induced by prolonged treatment with progesterone in dairy cows: an experimental model for the study of ovarian follicular cysts.Crossref | GoogleScholarGoogle Scholar |
Dupont, C, Cordier, AG, Junien, C, Mandon-Pépin, B, Levy, R, and Chavatte-Palmer, P (2012). Maternal environment and the reproductive function of the offspring. Theriogenology 78, 1405–1414.
| Maternal environment and the reproductive function of the offspring.Crossref | GoogleScholarGoogle Scholar |
Etchevers, L, Belotti, EM, Díaz, PU, Rodríguez, FM, Rey, F, Salvetti, NR, Ortega, HH, and Amweg, AN (2021). MC2R/MRAP2 activation could affect bovine ovarian steroidogenesis potential after ACTH treatment. Theriogenology 174, 102–113.
| MC2R/MRAP2 activation could affect bovine ovarian steroidogenesis potential after ACTH treatment.Crossref | GoogleScholarGoogle Scholar |
Evans, ACO, Mossa, F, Walsh, SW, Scheetz, D, Jimenez-Krassel, F, Ireland, JLH, Smith, GW, and Ireland, JJ (2012). Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reproduction in Domestic Animals 47, 31–37.
| Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring.Crossref | GoogleScholarGoogle Scholar |
Fernandes, I, Bastien, Y, Wai, T, Nygard, K, Lin, R, Cormier, O, Lee, HS, Eng, F, Bertos, NR, Pelletier, N, Mader, S, Han, VKM, Yang, X-J, and White, JH (2003). Ligand-dependent nuclear receptor corepressor LCoR functions by histone deacetylase-dependent and -independent mechanisms. Molecular Cell 11, 139–150.
| Ligand-dependent nuclear receptor corepressor LCoR functions by histone deacetylase-dependent and -independent mechanisms.Crossref | GoogleScholarGoogle Scholar |
Fouz, R, Gandoy, F, Sanjuán, ML, Yus, E, and Diéguez, FJ (2013). The use of crossbreeding with beef bulls in dairy herds: effects on calving difficulty and gestation length. Animal 7, 211–215.
| The use of crossbreeding with beef bulls in dairy herds: effects on calving difficulty and gestation length.Crossref | GoogleScholarGoogle Scholar |
Funston, RN, and Summers, AF (2013). Effect of prenatal programming on heifer development. Veterinary Clinics of North America: Food Animal Practice 29, 517–536.
| Effect of prenatal programming on heifer development.Crossref | GoogleScholarGoogle Scholar |
Gardiner-Garden, M, and Frommer, M (1987). CpG Islands in vertebrate genomes. Journal of Molecular Biology 196, 261–282.
| CpG Islands in vertebrate genomes.Crossref | GoogleScholarGoogle Scholar |
Gareis, NC, Angeli, E, Huber, E, Salvetti, NR, Rodríguez, FM, Ortega, HH, Hein, GJ, and Rey, F (2018). Alterations in key metabolic sensors involved in bovine cystic ovarian disease. Theriogenology 120, 138–146.
| Alterations in key metabolic sensors involved in bovine cystic ovarian disease.Crossref | GoogleScholarGoogle Scholar |
Garverick, HA, Juengel, JL, Smith, P, Heath, DA, Burkhart, MN, Perry, GA, Smith, MF, and McNatty, KP (2010). Development of the ovary and ontongeny of mRNA and protein for P450 aromatase (arom) and estrogen receptors (ER) α and β during early fetal life in cattle. Animal Reproduction Science 117, 24–33.
| Development of the ovary and ontongeny of mRNA and protein for P450 aromatase (arom) and estrogen receptors (ER) α and β during early fetal life in cattle.Crossref | GoogleScholarGoogle Scholar |
Hansen, PJ (2009). Effects of heat stress on mammalian reproduction. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 3341–3350.
| Effects of heat stress on mammalian reproduction.Crossref | GoogleScholarGoogle Scholar |
Hlaing, M, Nam, K, Lou, J, Pope, WF, and Nephew, KP (2001). Evidence for expression of estrogen receptor cofactor messenger ribonucleic acid in the ovary and uterus of domesticated animals (sheep, cow and pig). Life Sciences 68, 1427–1438.
| Evidence for expression of estrogen receptor cofactor messenger ribonucleic acid in the ovary and uterus of domesticated animals (sheep, cow and pig).Crossref | GoogleScholarGoogle Scholar |
Huber, E, Notaro, US, Recce, S, Rodríguez, FM, Ortega, HH, Salvetti, NR, and Rey, F (2020). Fetal programming in dairy cows: effect of heat stress on progeny fertility and associations with the hypothalamic-pituitary-adrenal axis functions. Animal Reproduction Science 216, 106348.
| Fetal programming in dairy cows: effect of heat stress on progeny fertility and associations with the hypothalamic-pituitary-adrenal axis functions.Crossref | GoogleScholarGoogle Scholar |
Hummitzsch, K, Anderson, RA, Wilhelm, D, Wu, J, Telfer, EE, Russell, DL, Robertson, SA, and Rodgers, RJ (2015). Stem cells, progenitor cells, and lineage decisions in the ovary. Endocrine Reviews 36, 65–91.
| Stem cells, progenitor cells, and lineage decisions in the ovary.Crossref | GoogleScholarGoogle Scholar |
Hummitzsch, K, Hatzirodos, N, Irving-Rodgers, HF, Hartanti, MD, Perry, VEA, Anderson, RA, and Rodgers, RJ (2019a). Morphometric analyses and gene expression related to germ cells, gonadal ridge epithelial-like cells and granulosa cells during development of the bovine fetal ovary. PLoS One 14, e0214130.
| Morphometric analyses and gene expression related to germ cells, gonadal ridge epithelial-like cells and granulosa cells during development of the bovine fetal ovary.Crossref | GoogleScholarGoogle Scholar |
Hummitzsch K, Irving-Rodgers HF, Schwartz J, Rodgers RJ (2019b) Development of the mammalian ovary and follicles. In ‘The ovary’. (Eds PCK Leung, EY Adashi) pp. 71–82. (Academic Press) https://doi.org/
| Crossref |
Hussein-Fikret, S, and Fuller, PJ (2005). Expression of nuclear receptor coregulators in ovarian stromal and epithelial tumours. Molecular and Cellular Endocrinology 229, 149–160.
| Expression of nuclear receptor coregulators in ovarian stromal and epithelial tumours.Crossref | GoogleScholarGoogle Scholar |
Isobe, N, and Yoshimura, Y (2007). Deficient proliferation and apoptosis in the granulosa and theca interna cells of the bovine cystic follicle. Journal of Reproduction and Development 53, 1119–1124.
| Deficient proliferation and apoptosis in the granulosa and theca interna cells of the bovine cystic follicle.Crossref | GoogleScholarGoogle Scholar |
Jia, M, Dahlman-Wright, K, and Gustafsson, JÅ (2015). Estrogen receptor alpha and beta in health and disease. Best Practice & Research Clinical Endocrinology & Metabolism 29, 557–568.
| Estrogen receptor alpha and beta in health and disease.Crossref | GoogleScholarGoogle Scholar |
Kinyamu, HK, and Archer, TK (2004). Modifying chromatin to permit steroid hormone receptor-dependent transcription. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 1677, 30–45.
| Modifying chromatin to permit steroid hormone receptor-dependent transcription.Crossref | GoogleScholarGoogle Scholar |
Klinge, CM (2000). Estrogen receptor interaction with co-activators and co-repressors. Steroids 65, 227–251.
| Estrogen receptor interaction with co-activators and co-repressors.Crossref | GoogleScholarGoogle Scholar |
Kuiper, GG, Enmark, E, Pelto-Huikko, M, Nilsson, S, and Gustafsson, JA (1996). Cloning of a novel receptor expressed in rat prostate and ovary. Proceedings of the National Academy of Sciences of the United States of America 93, 5925–5930.
| Cloning of a novel receptor expressed in rat prostate and ovary.Crossref | GoogleScholarGoogle Scholar |
Laporta, J, Fabris, TF, Skibiel, AL, Powell, JL, Hayen, MJ, Horvath, K, Miller-Cushon, EK, and Dahl, GE (2017). In utero exposure to heat stress during late gestation has prolonged effects on the activity patterns and growth of dairy calves. Journal of Dairy Science 100, 2976–2984.
| In utero exposure to heat stress during late gestation has prolonged effects on the activity patterns and growth of dairy calves.Crossref | GoogleScholarGoogle Scholar |
Laporta, J, Ferreira, FC, Ouellet, V, Dado-Senn, B, Almeida, AK, De Vries, A, and Dahl, GE (2020). Late-gestation heat stress impairs daughter and granddaughter lifetime performance. Journal of Dairy Science 103, 7555–7568.
| Late-gestation heat stress impairs daughter and granddaughter lifetime performance.Crossref | GoogleScholarGoogle Scholar |
Leonardsson, G, Jacobs, MA, White, R, Jeffery, R, Poulsom, R, Milligan, S, and Parker, M (2002). Embryo transfer experiments and ovarian transplantation identify the ovary as the only site in which nuclear receptor interacting protein 1/RIP140 action is crucial for female fertility. Endocrinology 143, 700–707.
| Embryo transfer experiments and ovarian transplantation identify the ovary as the only site in which nuclear receptor interacting protein 1/RIP140 action is crucial for female fertility.Crossref | GoogleScholarGoogle Scholar |
Liu, C, Peng, J, Matzuk, MM, and Yao, HH-C (2015). Lineage specification of ovarian theca cells requires multicellular interactions via oocyte and granulosa cells. Nature Communications 6, 6934.
| Lineage specification of ovarian theca cells requires multicellular interactions via oocyte and granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Livak, KJ, and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |
Lucy, MC, and Safranski, TJ (2017). Heat stress in pregnant sows: thermal responses and subsequent performance of sows and their offspring. Molecular Reproduction and Development 84, 946–956.
| Heat stress in pregnant sows: thermal responses and subsequent performance of sows and their offspring.Crossref | GoogleScholarGoogle Scholar |
McKenna, NJ, and O’Malley, BW (2002). Minireview: Nuclear receptor coactivators—an update. Endocrinology 143, 2461–2465.
| Minireview: Nuclear receptor coactivators—an update.Crossref | GoogleScholarGoogle Scholar |
Mcmillen, IC, and Robinson, JS (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiological Reviews 85, 571–633.
| Developmental origins of the metabolic syndrome: prediction, plasticity, and programming.Crossref | GoogleScholarGoogle Scholar |
Monniaux, D, Clément, F, Dalbiès-Tran, R, Estienne, A, Fabre, S, Mansanet, C, and Monget, P (2014). The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: what is the link? Biology of Reproduction 90, 85.
| The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: what is the link?Crossref | GoogleScholarGoogle Scholar |
Monteiro, APA, Guo, J-R, Weng, X-S, Ahmed, BM, Hayen, MJ, Dahl, GE, Bernard, JK, and Tao, S (2016). Effect of maternal heat stress during the dry period on growth and metabolism of calves. Journal of Dairy Science 99, 3896–3907.
| Effect of maternal heat stress during the dry period on growth and metabolism of calves.Crossref | GoogleScholarGoogle Scholar |
Mulac-Jericevic, B, and Conneely, OM (2004). Reproductive tissue selective actions of progesterone receptors. Reproduction 128, 139–146.
| Reproductive tissue selective actions of progesterone receptors.Crossref | GoogleScholarGoogle Scholar |
National Research Council (2021) ‘Nutrient Requirements of Dairy Cattle. 8th edn.’
Nilsson, EE, Maamar, MB, and Skinner, MK (2020). Environmentally induced epigenetic transgenerational inheritance and the Weismann barrier: the dawn of Neo-Lamarckian theory. Journal of Developmental Biology 8, 28.
| Environmentally induced epigenetic transgenerational inheritance and the Weismann barrier: the dawn of Neo-Lamarckian theory.Crossref | GoogleScholarGoogle Scholar |
Noriega-Reyes, MY, and Langley McCarron, E (2008). Correguladores del Receptor de Estrógenos y su Implicación en el Cáncer Mamario. Cancerología 3, 29–40.
O’Brien, ML, Park, K, In, Y, and Park-Sarge, O-K (1999). Characterization of estrogen receptor-β (ERβ) messenger ribonucleic acid and protein expression in rat granulosa cells. Endocrinology 140, 4530–4541.
| Characterization of estrogen receptor-β (ERβ) messenger ribonucleic acid and protein expression in rat granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Ortega, HH, Salvetti, NR, and Padmanabhan, V (2009). Developmental programming: prenatal androgen excess disrupts ovarian steroid receptor balance. Reproduction 137, 865–877.
| Developmental programming: prenatal androgen excess disrupts ovarian steroid receptor balance.Crossref | GoogleScholarGoogle Scholar |
Ouellet, V, Laporta, J, and Dahl, GE (2020). Late gestation heat stress in dairy cows: effects on dam and daughter. Theriogenology 150, 471–479.
| Late gestation heat stress in dairy cows: effects on dam and daughter.Crossref | GoogleScholarGoogle Scholar |
Park, S-E, Xu, J, Frolova, A, Liao, L, O’Malley, BW, and Katzenellenbogen, BS (2005). genetic deletion of the repressor of estrogen receptor activity (REA) enhances the response to estrogen in target tissues in vivo. Molecular and Cellular Biology 25, 1989–1999.
| genetic deletion of the repressor of estrogen receptor activity (REA) enhances the response to estrogen in target tissues in vivo.Crossref | GoogleScholarGoogle Scholar |
Park, CJ, Lin, P-C, Zhou, S, Barakat, R, Bashir, ST, Choi, JM, Cacioppo, JA, Oakley, OR, Duffy, DM, Lydon, JP, and Ko, CJ (2020). Progesterone receptor serves the ovary as a trigger of ovulation and a terminator of inflammation. Cell Reports 31, 107496.
| Progesterone receptor serves the ovary as a trigger of ovulation and a terminator of inflammation.Crossref | GoogleScholarGoogle Scholar |
Peterson, TJ, Karmakar, S, Pace, MC, Gao, T, and Smith, CL (2007). The silencing mediator of retinoic acid and thyroid hormone receptor (SMRT) corepressor is required for full estrogen receptor α transcriptional activity. Molecular and Cellular Biology 27, 5933–5948.
| The silencing mediator of retinoic acid and thyroid hormone receptor (SMRT) corepressor is required for full estrogen receptor α transcriptional activity.Crossref | GoogleScholarGoogle Scholar |
Pettersson, K, Delaunay, F, and Gustafsson, J-Å (2000). Estrogen receptor β acts as a dominant regulator of estrogen signaling. Oncogene 19, 4970–4978.
| Estrogen receptor β acts as a dominant regulator of estrogen signaling.Crossref | GoogleScholarGoogle Scholar |
Ranefall, P, Wester, K, Andersson, A-C, Busch, C, and Bengtsson, E (1998). Automatic quantification of immunohistochemically stained cell nuclei based on standard reference cells. Analytical Cellular Pathology 17, 111–123.
| Automatic quantification of immunohistochemically stained cell nuclei based on standard reference cells.Crossref | GoogleScholarGoogle Scholar |
Razin A, Shemer R (1999) Epigenetic control of gene expression. In ‘Genomic imprinting: an interdisciplinary approach. Results and problems in cell differentiation. Vol. 25’. (Ed. R Ohlsson) pp. 189–204. (Springer) https://doi.org/
| Crossref |
Recce, S, Huber, E, Notaro, US, Rodríguez, FM, Ortega, HH, Rey, F, Signorini, ML, and Salvetti, NR (2021). Association between heat stress during intrauterine development and the calving-to-conception and calving-to-first-service intervals in Holstein cows. Theriogenology 162, 95–104.
| Association between heat stress during intrauterine development and the calving-to-conception and calving-to-first-service intervals in Holstein cows.Crossref | GoogleScholarGoogle Scholar |
Rodríguez, FM, Salvetti, NR, Colombero, M, Stangaferro, ML, Barbeito, CG, Ortega, HH, and Rey, F (2013). Interaction between IGF1 and IGFBPs in bovine cystic ovarian disease. Animal Reproduction Science 140, 14–25.
| Interaction between IGF1 and IGFBPs in bovine cystic ovarian disease.Crossref | GoogleScholarGoogle Scholar |
Salvetti, NR, Stangaferro, ML, Palomar, MM, Alfaro, NS, Rey, F, Gimeno, EJ, and Ortega, HH (2010). Cell proliferation and survival mechanisms underlying the abnormal persistence of follicular cysts in bovines with cystic ovarian disease induced by ACTH. Animal Reproduction Science 122, 98–110.
| Cell proliferation and survival mechanisms underlying the abnormal persistence of follicular cysts in bovines with cystic ovarian disease induced by ACTH.Crossref | GoogleScholarGoogle Scholar |
Salvetti, NR, Alfaro, NS, Velázquez, MML, Amweg, AN, Matiller, V, Díaz, PU, and Ortega, HH (2012). Alteration in localization of steroid hormone receptors and coregulatory proteins in follicles from cows with induced ovarian follicular cysts. Reproduction 144, 723–735.
| Alteration in localization of steroid hormone receptors and coregulatory proteins in follicles from cows with induced ovarian follicular cysts.Crossref | GoogleScholarGoogle Scholar |
Skibiel, AL, Peñagaricano, F, Amorín, R, Ahmed, BM, Dahl, GE, and Laporta, J (2018). In utero heat stress alters the offspring epigenome. Scientific Reports 8, 14609.
| In utero heat stress alters the offspring epigenome.Crossref | GoogleScholarGoogle Scholar |
Tang, Z-R, Zhang, R, Lian, Z-X, Deng, S-L, and Yu, K (2019). Estrogen-receptor expression and function in female reproductive disease. Cells 8, 1123.
| Estrogen-receptor expression and function in female reproductive disease.Crossref | GoogleScholarGoogle Scholar |
Thompson, WE, Asselin, E, Branch, A, Stiles, JK, Sutovsky, P, Lai, L, Im, G-S, Prather, RS, Isom, SC, Rucker, E, and Tsang, BK (2004). Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary. Biology of Reproduction 71, 282–290.
| Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary.Crossref | GoogleScholarGoogle Scholar |
Turner, EH, Ng, SB, Nickerson, DA, and Shendure, J (2009). Methods for genomic partitioning. Annual Review of Genomics and Human Genetics 10, 263–284.
| Methods for genomic partitioning.Crossref | GoogleScholarGoogle Scholar |
Valtorta, SE, and Gallardo, MR (2004). Evaporative cooling for Holstein dairy cows under grazing conditions. International Journal of Biometeorology 48, 213–217.
| Evaporative cooling for Holstein dairy cows under grazing conditions.Crossref | GoogleScholarGoogle Scholar |
Wang, H, Eriksson, H, and Sahlin, L (2000). Estrogen receptors α and β in the female reproductive tract of the rat during the estrous cycle. Biology of Reproduction 63, 1331–1340.
| Estrogen receptors α and β in the female reproductive tract of the rat during the estrous cycle.Crossref | GoogleScholarGoogle Scholar |
Weaver, ICG, Cervoni, N, Champagne, FA, D’Alessio, AC, Sharma, S, Seckl, JR, Dymov, S, Szyf, M, and Meaney, MJ (2004). Epigenetic programming by maternal behavior. Nature Neuroscience 7, 847–854.
| Epigenetic programming by maternal behavior.Crossref | GoogleScholarGoogle Scholar |
Wei, LL, Hawkins, P, Baker, C, Norris, B, Sheridan, PL, and Quinn, PG (1996). An amino-terminal truncated progesterone receptor isoform, PRc, enhances progestin-induced transcriptional activity. Molecular Endocrinology 10, 1379–1387.
| An amino-terminal truncated progesterone receptor isoform, PRc, enhances progestin-induced transcriptional activity.Crossref | GoogleScholarGoogle Scholar |
White, R, Leonardsson, G, Rosewell, I, Ann Jacobs, M, Milligan, S, and Parker, M (2000). The nuclear receptor co-repressor Nrip1 (RIP140) is essential for female fertility. Nature Medicine 6, 1368–1374.
| The nuclear receptor co-repressor Nrip1 (RIP140) is essential for female fertility.Crossref | GoogleScholarGoogle Scholar |
Yang, MY, and Fortune, JE (2008). The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biology of Reproduction 78, 1153–1161.
| The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes.Crossref | GoogleScholarGoogle Scholar |
Yaşar, P, Ayaz, G, User, SD, Güpür, G, and Muyan, M (2017). Molecular mechanism of estrogen–estrogen receptor signaling. Reproductive Medicine and Biology 16, 4–20.
| Molecular mechanism of estrogen–estrogen receptor signaling.Crossref | GoogleScholarGoogle Scholar |
Zama, AM, and Uzumcu, M (2009). Fetal and neonatal exposure to the endocrine disruptor methoxychlor causes epigenetic alterations in adult ovarian genes. Endocrinology 150, 4681–4691.
| Fetal and neonatal exposure to the endocrine disruptor methoxychlor causes epigenetic alterations in adult ovarian genes.Crossref | GoogleScholarGoogle Scholar |
