Endocrine-Disrupting Chemicals and Their Effects during Female Puberty: A Review of Current Evidence

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Abstract

Puberty is the process of physical changes between childhood and adulthood during which adolescents reach sexual maturity and become capable of reproduction. It is considered one of the main temporal windows of susceptibility for the influence of the endocrine-disrupting chemicals (EDCs). EDCs may act as single chemical agents or as chemical mixtures; they can be pubertal influencers, accelerating and anticipating the processing of maturation of secondary sexual characteristics. Moreover, recent studies have started to point out how exposure to EDCs during puberty may predispose to breast cancer later in life. In fact, the estrogen-mimicking endocrine disruptors (EEDs) may influence breast tissue development during puberty in two main ways: the first is the action on the proliferation of the breast stromal cells, the second concerns epigenetic mechanisms. The aim of this mini-review was to better highlight what is new and what is not completely known regarding the role of EDCs during puberty.

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Most cited references 48

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EDC-2: The Endocrine Society's Second Scientific Statement on Endocrine-Disrupting Chemicals.

A Gore, V A Chappell, S Fenton … (2015)

The Endocrine Society's first Scientific Statement in 2009 provided a wake-up call to the scientific community about how environmental endocrine-disrupting chemicals (EDCs) affect health and disease. Five years later, a substantially larger body of literature has solidified our understanding of plausible mechanisms underlying EDC actions and how exposures in animals and humans-especially during development-may lay the foundations for disease later in life. At this point in history, we have much stronger knowledge about how EDCs alter gene-environment interactions via physiological, cellular, molecular, and epigenetic changes, thereby producing effects in exposed individuals as well as their descendants. Causal links between exposure and manifestation of disease are substantiated by experimental animal models and are consistent with correlative epidemiological data in humans. There are several caveats because differences in how experimental animal work is conducted can lead to difficulties in drawing broad conclusions, and we must continue to be cautious about inferring causality in humans. In this second Scientific Statement, we reviewed the literature on a subset of topics for which the translational evidence is strongest: 1) obesity and diabetes; 2) female reproduction; 3) male reproduction; 4) hormone-sensitive cancers in females; 5) prostate; 6) thyroid; and 7) neurodevelopment and neuroendocrine systems. Our inclusion criteria for studies were those conducted predominantly in the past 5 years deemed to be of high quality based on appropriate negative and positive control groups or populations, adequate sample size and experimental design, and mammalian animal studies with exposure levels in a range that was relevant to humans. We also focused on studies using the developmental origins of health and disease model. No report was excluded based on a positive or negative effect of the EDC exposure. The bulk of the results across the board strengthen the evidence for endocrine health-related actions of EDCs. Based on this much more complete understanding of the endocrine principles by which EDCs act, including nonmonotonic dose-responses, low-dose effects, and developmental vulnerability, these findings can be much better translated to human health. Armed with this information, researchers, physicians, and other healthcare providers can guide regulators and policymakers as they make responsible decisions.

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Parent-of-origin specific allelic associations among 106 genomic loci for age at menarche

John RB Perry, Felix Day, Cathy E Elks … (2014)

Age at menarche is a marker of timing of puberty in females. It varies widely between individuals, is a heritable trait and is associated with risks for obesity, type 2 diabetes, cardiovascular disease, breast cancer and all-cause mortality 1 . Studies of rare human disorders of puberty and animal models point to a complex hypothalamic-pituitary-hormonal regulation 2,3 , but the mechanisms that determine pubertal timing and underlie its links to disease risk remain unclear. Here, using genome-wide and custom-genotyping arrays in up to 182,416 women of European descent from 57 studies, we found robust evidence (P<5×10−8) for 123 signals at 106 genomic loci associated with age at menarche. Many loci were associated with other pubertal traits in both sexes, and there was substantial overlap with genes implicated in body mass index and various diseases, including rare disorders of puberty. Menarche signals were enriched in imprinted regions, with three loci (DLK1/WDR25, MKRN3/MAGEL2 and KCNK9) demonstrating parent-of-origin specific associations concordant with known parental expression patterns. Pathway analyses implicated nuclear hormone receptors, particularly retinoic acid and gamma-aminobutyric acid-B2 receptor signaling, among novel mechanisms that regulate pubertal timing in humans. Our findings suggest a genetic architecture involving at least hundreds of common variants in the coordinated timing of the pubertal transition.

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Secondary Sexual Characteristics and Menses in Young Girls Seen in Office Practice: A Study from the Pediatric Research in Office Settings Network

M E Herman-Giddens, E J Slora, R. Wasserman … (1997)

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Journal

Journal ID (nlm-ta): Int J Mol Sci

Journal ID (iso-abbrev): Int J Mol Sci

Journal ID (publisher-id): ijms

Title: International Journal of Molecular Sciences

Publisher: MDPI

ISSN (Electronic): 1422-0067

Publication date (Electronic): 18 March 2020

Publication date Collection: March 2020

Volume: 21

Issue: 6

Electronic Location Identifier: 2078

Affiliations

[1 ]Neonatal Intensive Care Unit, Department of Medical and Surgical Sciences of the Mothers, Children and Adults, University of Modena and Reggio Emilia, via del Pozzo 71, 41124 Modena, Italy; natascia.bertoncelli@ 123456gmail.com (N.B.); alberto.berardi@ 123456unimore.it (A.B.)

[2 ]Post Graduate School of Paediatrics, Department of Medical and Surgical Sciences of the Mothers, Children and Adults, University of Modena and Reggio Emilia, via del Pozzo 71, 41124 Modena, Italy; viola.trevisani@ 123456gmail.com (V.T.); luciamarrozzini@ 123456gmail.com (L.M.); lorenzo.iughetti@ 123456unimore.it (L.I.)

[3 ]Pediatric Unit, Department of Medical and Surgical Sciences of the Mothers, Children and Adults, University of Modena and Reggio Emilia, via del Pozzo 71, 41124 Modena, Italy; barbara.predieri@ 123456unimore.it

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[* ]Correspondence: laura.lucaccioni@ 123456unimore.it ; Tel.: +39-0594223254

Author information

Natascia Bertoncelli https://orcid.org/0000-0001-9275-8801

Barbara Predieri https://orcid.org/0000-0002-3302-6886

Lorenzo Iughetti https://orcid.org/0000-0003-0370-7872

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Publisher ID: ijms-21-02078

DOI: 10.3390/ijms21062078

PMC ID: 7139481

PubMed ID: 32197344

SO-VID: 78d47e95-40e1-4633-9c02-9fbea85a2995

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Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

Endocrine-Disrupting Chemicals and Their Effects during Female Puberty: A Review of Current Evidence

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Higher order chromatin architecture

Most cited references 48

EDC-2: The Endocrine Society's Second Scientific Statement on Endocrine-Disrupting Chemicals.

Parent-of-origin specific allelic associations among 106 genomic loci for age at menarche

Secondary Sexual Characteristics and Menses in Young Girls Seen in Office Practice: A Study from the Pediatric Research in Office Settings Network

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