Mechanisms of intergenerational transmission of polycystic ovary syndrome

Dumesic, Daniel A; Hoyos, Luis R; Chazenbalk, Gregorio D; Naik, Rajanigandha; Padmanabhan, Vasantha; Abbott, David H

doi:10.1530/rep-19-0197

Cited by 101Ovarian function and disordersBirth, Development, and HealthReproductive Biology and Fertility

Mechanisms of intergenerational transmission of polycystic ovary syndrome

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Dumesic, Daniel A, Hoyos, Luis R, Chazenbalk, Gregorio D, Naik, Rajanigandha, Padmanabhan, Vasantha, Abbott, David H·2020·Reproduction

DOI 10.1530/rep-19-0197PMC PMC6989388

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Abstract

Developmental origins of adult disease (DoHAD) refers to critical gestational ages during human fetal development and beyond when the endocrine metabolic status of the mother can permanently program the physiology and/or morphology of the fetus, modifying its susceptibility to disease after birth. The aim of this review is to address how DoHAD plays an important role in the phenotypic expression of polycystic ovary syndrome (PCOS), the most common endocrinopathy of women characterized by hyperandrogenism, oligo-anovulation and polycystic ovarian morphology. Clinical studies of PCOS women are integrated with findings from relevant animal models to show how intergenerational transmission of these central components of PCOS are programmed through an altered maternal endocrine–metabolic environment that adversely affects the female fetus and long-term offspring health. Prenatal testosterone treatment in monkeys and sheep have been particularly crucial in our understanding of developmental programming of PCOS because organ system differentiation in these species, as in humans, occurs during fetal life. These animal models, along with altricial rodents, produce permanent PCOS-like phenotypes variably characterized by LH hypersecretion from reduced steroid-negative feedback, hyperandrogenism, ovulatory dysfunction, increased adiposity, impaired glucose-insulin homeostasis and other metabolic abnormalities. The review concludes that DoHAD underlies the phenotypic expression of PCOS through an altered maternal endocrine–metabolic environment that can induce epigenetic modifications of fetal genetic susceptibility to PCOS after birth. It calls for improved maternal endocrine–metabolic health of PCOS women to lower their risks of pregnancy-related complications and to potentially reduce intergenerational susceptibility to PCOS and its metabolic derangements in offspring.

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Epigenetic reprogramming of germ-line cells can lead to transgenerational inheritance resulting in phenotypic variation or pathology in the absence of continued direct exposure.
“In addition, epigenetic reprogramming of germ-line cells can lead to transgenerational inheritance resulting in phenotypic variation or pathology in the absence of continued direct exposure [98].”
From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [98]
The Endocrine antecedents of PCOS section says epigenomic remodeling can be inherited across generations through nongenetic mechanisms, and the Conclusion suggests fetal epigenetic changes may contribute to PCOS. Neither passage identifies germ-line cell reprogramming as the mechanism or establishes inheritance in the absence of continued direct exposure. (LLM, conf=0.83)
Experimental — accuracy not yet measured
These factors include hormones, vitamins, diet-derived metabolites and environmental chemicals.
“These include hormones, vitamins, diet-derived metabolites and environmental chemicals [48,98,103,104].”
From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [98]
The Introduction and Placental aromatization sections discuss maternal nutrition and hormones as influences on fetal development. The passages do not identify vitamins, diet-derived metabolites or environmental chemicals as factors, so the full list is not supported. Page numbers were not available in our copy. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Compelling evidence shows that a wide range of maternal, nutritional and environmental factors can affect fetal development during critical periods of programming.
“Compelling evidence shows that a wide range of maternal, nutritional and environmental factors can effect fetal development during these critical periods of programming [44,98,99,101,102].”
From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [98]
Multiple lines of evidence suggest that inherited PCOS gene variants are developmentally programmed in a way that primes them for activation by nutritional and environmental factors in postnatal life.
“In keeping with this model, multiple lines of evidence suggest that inherited PCOS gene variants are developmentally programmed in a way that primes them for activation by nutritional and environmental factors in postnatal life [41,42,98].”
From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [98]

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Infants of Women with Polycystic Ovary Syndrome Have Lower Cord Blood Androstenedione and Estradiol Levels
Anderson, H., Fogel, N. R., Grebe, S. K. G., Singh, R. J., Taylor, R. L., & Dunaif, A. E. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2651 · Cited by 118 · see citing works
Impaired Adipocyte Lipolysis in Nonobese Women with the Polycystic Ovary Syndrome: A Possible Link to Insulin Resistance?1
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Androgens in maternal vascular and placental function: implications for preeclampsia pathogenesis
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Impaired Developmental Competence of Oocytes in Adult Prenatally Androgenized Female Rhesus Monkeys Undergoing Gonadotropin Stimulation for in Vitro Fertilization
Dumesic, D. A., Schramm, R. D., Peterson, E., Paprocki, A. M., Zhou, R., & Abbott, D. H. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.3.8287 · Cited by 105 · see citing works
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Fetal Programming: Excess Prenatal Testosterone Reduces Postnatal Luteinizing Hormone, But Not Follicle-Stimulating Hormone Responsiveness, to Estradiol Negative Feedback in the Female
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Endocrine Antecedents of Polycystic Ovary Syndrome in Fetal and Infant Prenatally Androgenized Female Rhesus Monkeys1
Abbott, D. H., Barnett, D. K., Levine, J. E., Padmanabhan, V., Dumesic, D. A., Jacoris, S., & Tarantal, A. F. (2008) · Biology of Reproduction · doi:10.1095/biolreprod.108.067702 · Cited by 102 · see citing works
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Timing of Prenatal Androgen Exposure: Anatomical and Endocrine Effects on Juvenile Male and Female Rhesus Monkeys
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Growth and development of adipose tissue
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Prevalence of Type II diabetes mellitus and insulin resistance in parents of women with polycystic ovary syndrome
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Effects of testosterone on fat cell lipolysis. Species differences and possible role in polycystic ovarian syndrome
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Experimentally induced gestational androgen excess disrupts glucoregulation in rhesus monkey dams and their female offspring
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Adipose Insulin Resistance in Normal-Weight Women With Polycystic Ovary Syndrome
Dumesic, D. A., Phan, J. D., Leung, K. L., Grogan, T. R., Ding, X., Li, X., Hoyos, L. R., Abbott, D. H., & Chazenbalk, G. D. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-02086 · Cited by 92 · see citing works
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Role of first trimester HbA1c as a predictor of adverse obstetric outcomes in a multi-ethnic cohort.
Mañé, L., Flores-Le Roux, J. A., Benaiges, D., Rodríguez, M., Marcelo, I., Chillarón, J. J., Pedro-Botet, J., Llauradó, G., Gortazar, L., Carreras, R., et al. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-2581 · Cited by 91 · see citing works
Hypertension caused by prenatal testosterone excess in female sheep
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Abnormal Expression of Genes Involved in Inflammation, Lipid Metabolism, and Wnt Signaling in the Adipose Tissue of Polycystic Ovary Syndrome
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Birth weight and age at menarche in patients with polycystic ovary syndrome or diminished ovarian reserve, in a retrospective cohort
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Hyperandrogenism and Hyperinsulinism in Children of Women with Polycystic Ovary Syndrome: A Controlled Study
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Intrauterine Environment and Polycystic Ovary Syndrome
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Low-Grade Chronic Inflammation in Pregnant Women With Polycystic Ovary Syndrome: A Prospective Controlled Clinical Study
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Placental characteristics in women with polycystic ovary syndrome
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Polycystic ovary syndrome is associated with anogenital distance, a marker of prenatal androgen exposure
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Developmental Programming: Follicular Persistence in Prenatal Testosterone-Treated Sheep Is Not Programmed by Androgenic Actions of Testosterone
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Epigenetic modifications of the Zfp/ZNF423 gene control murine adipogenic commitment and are dysregulated in human hypertrophic obesity
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Lipid profile in nonobese pregnant women with polycystic ovary syndrome: A prospective controlled clinical study
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Interactive Effects of Vinclozolin and Testosterone Propionate on Pregnancy and Sexual Differentiation of the Male and Female SD Rat
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Higher luteinizing hormone levels associated with antimüllerian hormone in postmenarchal daughters of women with polycystic ovary syndrome
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Introducing a rat model of prenatal androgen‐induced polycystic ovary syndrome in adulthood
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Developmental Programming: Impact of Gestational Steroid and Metabolic Milieus on Adiposity and Insulin Sensitivity in Prenatal Testosterone-Treated Female Sheep
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Fetal development of subcutaneous white adipose tissue is dependent on Zfp423
Shao, M., Hepler, C., Vishvanath, L., MacPherson, K. A., Busbuso, N. C., & Gupta, R. K. (2016) · Molecular Metabolism · doi:10.1016/j.molmet.2016.11.009 · Cited by 67 · see citing works
Developmental Programming: Impact of Prenatal Testosterone Excess on Insulin Sensitivity, Adiposity, and Free Fatty Acid Profile in Postpubertal Female Sheep
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Prenatal Androgen Exposure Leads to Alterations in Gene and Protein Expression in the Ovine Fetal Ovary
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Improvement of hyperandrogenism and hyperinsulinemia during pregnancy in women with polycystic ovary syndrome: possible effect in the ovarian follicular mass of their daughters
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Presence of polycystic ovary syndrome is associated with longer anogenital distance in adult Mediterranean women
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Human Fetal Ovary Development Involves the Spatiotemporal Expression of P450c17 Protein
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Impaired preadipocyte differentiation into adipocytes in subcutaneous abdominal adipose of PCOS-like female rhesus monkeys
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Pre-Conception Characteristics Predict Obstetrical and Neonatal Outcomes in Women With Polycystic Ovary Syndrome
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Developmental programing: impact of testosterone on placental differentiation
Beckett, E. M., Astapova, O., Steckler, T. L., Veiga‐Lopez, A., & Padmanabhan, V. (2014) · Reproduction · doi:10.1530/rep-14-0055 · Cited by 55 · see citing works
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Early trophoblast invasion and placentation in women with different PCOS phenotypes.
Palomba, S., Falbo, A., Chiossi, G., Tolino, A., Tucci, L., Sala, G. L. L., & Zullo, F. (2014) · Reproductive Biomedicine Online · doi:10.1016/j.rbmo.2014.04.010 · Cited by 55 · see citing works
Developmental Programming: Prenatal and Postnatal Androgen Antagonist and Insulin Sensitizer Interventions Prevent Advancement of Puberty and Improve LH Surge Dynamics in Prenatal Testosterone-Treated Sheep
Padmanabhan, V., Veiga‐Lopez, A., Herkimer, C., Salloum, B. A., Moeller, J., Beckett, E. M., & Sreedharan, R. (2015) · Endocrinology · doi:10.1210/en.2015-1235 · Cited by 54 · see citing works
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Prenatal exposure to excess testosterone modifies the developmental trajectory of the insulin‐like growth factor system in female sheep
Crespi, E. J., Steckler, T. L., MohanKumar, P. S., & Padmanabhan, V. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.103929 · Cited by 53 · see citing works
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Developmental Programming: Exposure to Testosterone Excess Disrupts Steroidal and Metabolic Environment in Pregnant Sheep
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A novel method to demonstrate that pregnant women with polycystic ovary syndrome hyper-expose their fetus to androgens as a possible stepping stone for the developmental theory of PCOS. A pilot study
Homburg, R., Gudi, A., Shah, A. M., & Layton, A. (2017) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-017-0282-1 · Cited by 51 · see citing works
Diabetes mellitus and insulin resistance in mothers, fathers, sisters, and brothers of women with polycystic ovary syndrome: a systematic review and meta-analysis
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Pioglitazone improves insulin action and normalizes menstrual cycles in a majority of prenatally androgenized female rhesus monkeys
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Prenatal programming: adverse cardiac programming by gestational testosterone excess
Vyas, A. K., Hoang, V., Padmanabhan, V., Gilbreath, E., & Mietelka, K. A. (2016) · Scientific Reports · doi:10.1038/srep28335 · Cited by 48 · see citing works
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Developmental programming in sheep: Administration of testosterone during 60–90 days of pregnancy reduces breeding success and pregnancy outcome
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Prenatal Exposure of the Ovine Fetus to Androgens Sexually Differentiates the Steroid Feedback Mechanisms That Control Gonadotropin Releasing Hormone Secretion and Disrupts Ovarian Cycles
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Prenatal testosterone propionate and postnatal ovarian activity in the rat
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Prenatal androgen excess negatively impacts body fat distribution in a nonhuman primate model of polycystic ovary syndrome
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Circulating maternal testosterone concentrations at 18 weeks of gestation predict circulating levels of antimüllerian hormone in adolescence: a prospective cohort study
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Polycystic Ovary Syndrome and Hyperandrogenic States
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Precocious subcutaneous abdominal stem cell development to adipocytes in normal-weight women with polycystic ovary syndrome
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Comparison of the metabolic parameters and androgen level of umbilical cord blood in newborns of mothers with polycystic ovary syndrome and controls.
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Elevated concentrations of the β-subunit of human chorionic gonadotropin and testosterone in the amniotic fluid of gestations of diabetic mothers
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Gestational Weight Gain in Women With Polycystic Ovary Syndrome: A Controlled Study.
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Early prenatal androgenization results in diminished ovarian reserve in adult female rhesus monkeys
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Normal Pubertal Development in Daughters of Women With PCOS: A Controlled Study
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Developmental Programming: Impact of Prenatal Testosterone Excess on Steroidal Machinery and Cell Differentiation Markers in Visceral Adipocytes of Female Sheep
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Differential rate in decline in ovarian reserve markers in women with polycystic ovary syndrome compared with control subjects: results of a longitudinal study
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The Effect of Trophic Agents on Fetal Ovarian Steroidogenesis in Organ Culture
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Accelerated Episodic Luteinizing Hormone Release Accompanies Blunted Progesterone Regulation in PCOS-like Female Rhesus Monkeys (Macaca Mulatta) Exposed to Testosterone during Early-to-Mid Gestation
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Progesterone Suppression of Luteinizing Hormone Pulse Frequency in Adolescent Girls With Hyperandrogenism: Effects of Metformin
Lundgren, J. A., Kim, S. H., Solorzano, C. M. B., McCartney, C. R., & Marshall, J. C. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-02068 · Cited by 11 · see citing works
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Insulin resistance and PCOS: chicken or egg?
Moghetti, P., & Tosi, F. (2021) · Journal of Endocrinological Investigation · doi:10.1007/s40618-020-01351-0 · Cited by 209 · see citing works
Anti-Müllerian Hormone in Female Reproduction
di Clemente, N., Racine, C., Pierre, A., & Taieb, J. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnab012 · Cited by 201 · see citing works
Fundamental Concepts and Novel Aspects of Polycystic Ovarian Syndrome: Expert Consensus Resolutions
Aversa, A., Vignera, S. L., Rago, R., Gambineri, A., Nappi, R. E., Calogero, A. E., & Ferlin, A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00516 · Cited by 159 · see citing works
A Review on CYP11A1, CYP17A1, and CYP19A1 Polymorphism Studies: Candidate Susceptibility Genes for Polycystic Ovary Syndrome (PCOS) and Infertility
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Pathophysiology of polycystic ovary syndrome revisited: Current understanding and perspectives regarding future research
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“Fetal ovaries also respond to maternal hyperinsulinemia, evident in women with diabetes or PCOS, by upregulating androgen production, representing a maternal– fetal interaction that increases overall testosterone exposure (Dumesic et al., 2020).”
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Polycystic ovary syndrome (PCOS) increases the risk of subsequent gestational diabetes mellitus (GDM): A novel therapeutic perspective
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The Goto-Kakizaki rat is a spontaneous prototypical rodent model of polycystic ovary syndrome
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The Search for the Causes of Common Hyperandrogenism, 1965 to Circa 2015
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Intergenerational Influences between Maternal Polycystic Ovary Syndrome and Offspring: An Updated Overview
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Genes in loci genetically associated with polycystic ovary syndrome are dynamically expressed in human fetal gonadal, metabolic and brain tissues
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Prenatal Androgen Excess Induces Multigenerational Effects on Female and Male Descendants
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Biochemical Characterization and Molecular Determination of Estrogen Receptor-α (ESR1 PvuII-rs2234693 T>C) and MiRNA-146a (rs2910164 C>G) Polymorphic Gene Variations and Their Association with the Risk of Polycystic Ovary Syndrome
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Shapes of the uterine cavity are different in women with polycystic ovary syndrome
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Therapeutic potentials of the caffeine in polycystic ovary syndrome in a rat model
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A blocking antibody against anti-Müllerian hormone restores ovulation and normal androgen levels in a spontaneous rat model of polycystic ovary syndrome
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New insights into the relationship of antimüllerian hormone with polycystic ovary syndrome and its diagnostic accuracy: an updated and extended meta-analysis using a marginal beta-binomial model
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Association of rs13429458 and rs12478601 Single Nucleotide Polymorphisms of THADA Gene with Polycystic Ovary Syndrome.
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Ovarian expression of follicle stimulating hormone and activin receptors genes in a prenatally-androgenized rat model of polycystic ovary syndrome in adulthood
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Impaired Mitochondrial Biogenesis Inhibits Epithelial-Mesenchymal Transition in Villi of PCOS Patients
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Reduced miR-338-3p contributes to polycystic ovarian syndrome by inhibiting proliferation and enhancing apoptosis
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The Impact of Microparticulate Air Pollution in Polycystic Ovary Syndrome: A Narrative Review
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Sex Differences in Migraine: A Twin Study
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Special Considerations on Hyperandrogenism and Insulin Resistance in Nonobese Polycystic Ovaries Syndrome
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Does a compromised placenta contribute to transgenerational transmission of metabolic dysfunction in polycystic ovary syndrome?
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PCOS as a generational disease - risks to mother and children
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ESR2 Regulates Granulosa Cell Proliferation and Steroidogenesis via the PI3K/AKT/mTOR Signaling Pathway in Wuding Chickens
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Study the effect of Kisspeptin 1 on polycystic ovarian syndrome PCOS and obesity in Iraqi women patients
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Découverte du premier modèle pré-clinique développant spontanément un syndrome des ovaires polykystiques
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Therapeutic potentials of the caffeine in polycystic ovary syndrome in a rat model: via modulation of proinflammatory cytokines and antioxidant activity Running title: The effects of caffeine on rats with polycystic ovary syndromePreprint
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Self-citation

Authors: Dumesic, D. A., Hoyos, L. R., Chazenbalk, G. D., Naik, R., Padmanabhan, V., & Abbott, D. H.
Affiliations: University of California, Los Angeles (US)
University of Michigan (US)
University of Wisconsin–Madison (US)
Corresponding author: Dumesic, Daniel A
ORCID: Dumesic, Daniel A
Hoyos, Luis R
Chazenbalk, Gregorio D
Padmanabhan, Vasantha
Abbott, David H
Venue: Reproduction
Publisher: Oxford University Press (OUP)
Published: 2020-01-01
Volume: 159
Issue: 1
Pages: R1-R13
ISSN: 1470-1626 (ISSN-L)
1741-7899
DOI: 10.1530/rep-19-0197
PMC: PMC6989388
OpenAlex: W2965641758
Semantic Scholar: f67e23f78ce75551f4e1946f0631e03f0001631a
Cited by: 101
References: 138
Citations by year: 2026: 7 · 2025: 13 · 2024: 10 · 2023: 18 · 2022: 19 · 2021: 20 · 2020: 13
FWCI: 1.83
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: Reproduction (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: University of Michigan
University of Virginia (P50HD028934)
National Institutes of Health (P51 ODO11092, P51OD011092, UL1TR001881)
Oregon National Primate Research Center (P51 ODO11092)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK020572)
National Center for Advancing Translational Sciences (UCLA CTSI Grant Number UL1TR001881)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P50HD071836, P01HD044232, P50HD028934)
Clinical and Translational Science Institute, University of California, Los Angeles (UL1 TR001881)
Topics: Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Keywords: polycystic ovary syndrome, intergenerational transmission, developmental origins of adult disease, fetal programming, hyperandrogenism, epigenetic modifications, maternal health, pregnancy complications, ovulatory dysfunction, insulin resistance
MeSH terms: Female, Humans, Polycystic Ovary Syndrome, Intergenerational Relations, Infectious Disease Transmission, Vertical

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Mechanisms of intergenerational transmission of polycystic ovary syndrome

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