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Zane Cutright Inman Department of Comparative Biosciences, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

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Jodi A Flaws Department of Comparative Biosciences, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

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In brief

This review article highlights the associations between endocrine-disrupting chemicals, reproductive aging, and menopause. Collectively, the current literature indicates that phthalates, bisphenols, parabens, per- and poly-fluoroalkyl substances, polychlorinated biphenyls, dioxins, and pesticides are associated with reproductive aging in women and animal models.

Abstract

Menopause marks the end of a woman’s reproductive lifetime and can have a significant effect on a woman’s quality of life. Menopause naturally occurs at 51 years of age on average, but recent literature suggests that endocrine-disrupting chemicals (EDCs) in our environment can accelerate reproductive aging, causing women to reach menopause at earlier ages. This is concerning as menopause can significantly alter a woman’s quality of life and is associated with increased risks of conditions such as depression, osteoporosis, and cardiovascular disease. EDC exposures have also been associated with more intense menopausal symptoms, making the menopausal transition more difficult for some women. This review highlights the associations between EDC exposure, early menopause, and reproductive aging, using both epidemiological and experimental studies.

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Katie J Danielson Department of Biochemistry and Molecular Biology, University of British Columbia, Health Sciences Mall, Vancouver, British Columbia, Canada

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Kayla L Judson Department of Biochemistry and Molecular Biology, University of British Columbia, Health Sciences Mall, Vancouver, British Columbia, Canada

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Ethan J Greenblatt Department of Biochemistry and Molecular Biology, University of British Columbia, Health Sciences Mall, Vancouver, British Columbia, Canada

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In Brief

This point of view article focuses on the potential contribution of defects in protein synthesis (translation) to the incidence of oocyte meiotic failure. We discuss the potential cause of diminished oocyte translation during aging and the impact of these deficits on the function of the meiotic spindle.

Abstract

Errors during female meiosis lead to embryonic aneuploidy and miscarriage and occur with increasing frequency during aging. The underlying molecular changes that drive female meiotic instability remain a subject of debate. Developing oocytes undergo a tremendous increase in cytoplasmic volume over several months of follicle development and rely on long-lived mRNAs and ribosomes accumulated during this growth phase for subsequent meiotic maturation. In this point of view article, we discuss how the unique reliance on stores of long-lived mRNAs and ribosomes may represent an Achilles' heel for oocyte function and how alterations that reduce the translational capacity of oocytes could be a factor significantly contributing to female infertility. Understanding these mechanisms could lead to new therapeutic strategies to improve fertility outcomes.

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Ruth Chan-Sui Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, USA
Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, Michigan, USA

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Robin E Kruger Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, Michigan, USA

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Evelyn Cho Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, USA

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Vasantha Padmanabhan Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, Michigan, USA
Department of Pediatrics, University of Michigan, Ann Arbor, Michigan, USA
Department of Molecular & Integrative Physiology, University of Michigan, Ann Arbor, Michigan, USA

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Molly Moravek Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, Michigan, USA
Department of Urology, University of Michigan, Ann Arbor, Michigan, USA
Cellular and Molecular Biology Program, University of Michigan, Ann Arbor, Michigan, USA
Department of Women's Heath, Henry Ford Health, Rochester Hills, Michigan, USA

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Ariella Shikanov Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, USA
Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, Michigan, USA
Cellular and Molecular Biology Program, University of Michigan, Ann Arbor, Michigan, USA

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In brief

Animal studies are needed to inform clinical guidance on the effects of testosterone gender-affirming hormone therapy (T-GAHT) on fertility. This review summarizes current animal models of T-GAHT and identifies gaps in knowledge for future study.

Abstract

Testosterone gender affirming hormone therapy (T-GAHT) is frequently used by transgender and gender-diverse individuals assigned female at birth to establish masculinizing characteristics. Although many seek parenthood, particularly as a gestational parent or through surrogacy, the current standard guidance of fertility counseling for individuals on testosterone (T) lacks clarity. At this time, individuals are typically recommended to undergo fertility preservation or stop treatment, associating T-therapy with a loss of fertility; however, there is an absence of consistent information regarding the true fertility potential for transgender and gender-diverse adults and adolescents. This review evaluates recent studies that utilize animal models of T-GAHT to relate to findings from clinical studies, with a more specific focus on fertility. Relevant literature based on murine models in post- and pre-pubertal populations has suggested reversibility of the impacts of T-GAHT, alone or following gonadotropin-releasing hormone agonist (GnRHa), on reproduction. These studies reported changes in clitoral area and ovarian morphology, including corpora lutea, follicle counts, and ovarian weights from T-treated mice. Future studies should aim to determine the impact of the duration of T-treatment and cessation on fertility outcomes, as well as establish animal models that are clinically representative of these outcomes with respect to gender diverse populations.

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Peter Cummings Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA

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Angela Lawson Department of Obstetrics and Gynecology, Northwestern University, Chicago, Illinois, USA

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In brief

Transgender and gender-diverse (TGD) people have similar desires for parenting as cisgender individuals but are likely to face greater barriers in accessing fertility treatment than their cisgender peers. Mental health professionals are well-positioned to advocate for and support TGD individuals seeking fertility care through pre-fertility treatment implications counseling regarding the psychosocial aspects of fertility treatment and family building.

Abstract

Transgender and gender-diverse (TGD) individuals experience significantly greater all-cause mortality and mental health disparities compared to their cisgender peers. Gender-affirming hormone therapy (GAHT) is a safe and effective treatment option for gender dysphoria that dramatically improves psychosocial health outcomes but may adversely impact fertility. Medical society guidelines recommend medical fertility preservation (FP) counseling and pre-fertility treatment psychoeducational implications consultation from qualified, reproductive mental health professionals (MHPs) for TGD individuals pursuing FP or third-party reproductive treatment. However, sparse literature exists specific to the structure of mental health psychoeducational consultation for TGD individuals pursuing FP. This narrative review highlights important areas for discussion in pre-fertility treatment mental health consultations. Results indicate that implications counseling should be conducted by an MHP with specialized training in reproductive mental health with TGD populations to reduce the risk of harm and promote successful emotional navigation of fertility treatment. Such counseling should be psychoeducational and not gatekeeping in nature and may include consideration of the psychosocial (e.g. emotional, relational, ethical, spiritual, social) risks and benefits of various family-building options. During these consultations, TGD individuals can explore their hopes and fears related to fertility and future family-building plans and discuss realistic treatment expectations, individual strengths, coping and communication strategies, and identify key support network members who may aid in navigating the fertility treatment process. MHPs can provide referrals to appropriate resources if necessary to help TGD individuals navigate treatment while coping with psychological symptoms and promoting behavior change.

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Mick van Trotsenburg Sigmund Freud Private University, Freudplatz, Vienna, Austria

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In brief

This manuscript aims to promote an understanding of the special needs of transgender and gender-diverse people by putting trans gynecology into context. By definition, medical interventions for transgender people are not different from the treatment of cisgender people but cannot be singled out as gender-affirmative treatment. Treatment is dedicated to an overarching goal beyond medicine, namely to enable and maintain social functioning under the signs of the social gender. It is therefore that this narrative overview intensively deals with the requirements of trans gynecology. Also, various gynecological disorders are touched upon, provided they are relevant to trans people. The different significance of gynecological symptoms for either trans men or trans women, and the effects of supraphysiological androgen treatment on hormone-sensitive tissue, are stressed.

Abstract

Transgender health care is not just gender-affirmative transitional care but is committed to a superior objective, often beyond a medical perspective: to create and maintain physical conditions for social functioning under the signs of the individually appropriate sex and to contribute to significantly reducing gender dysphoria. For these purposes, it is a prerequisite to have a distinct contextual understanding of the complex reality of transpeople and knowledge about the numerous facets of transgender healthcare. Gynecology for transgender and gender-diverse people does not differ greatly from gynecology for cisgender female patients except in goals and context. Relief from complaints derived from genital organs is, of course important, but for transpeople there always is an overarching gender dimension that sometimes complicates treatment and might give rise to misunderstandings. Also, minority stress caused by societal factors frequently impacts the mental and physical state of health negatively and needs to be considered. This paper focuses on the context of trans gynecology and addresses various contentual aspects for both transmale patients having left genital organs in situ and transfemale patients with gynecological demands. Gynecological topics are addressed, highlighting their relevance for transgender and gender-diverse people (TGD), including the effects of supra-physiological androgen exposure on ovaries and uterus, vaginal bleeding, pelvic pain under testosterone treatment, screening policies, and benign gynecological disorders as clinical manifestations may appear differently and treatment may be more burdensome.

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Cecilia Lucia Centola Centro de Investigaciones Endocrinológicas “Dr. César Bergadá” (CEDIE) CONICET - FEI - División de Endocrinología, Hospital de Niños Ricardo Gutiérrez, Gallo 1330, Ciudad Autónoma de Buenos Aires, Argentina

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Marina Ercilia Dasso Centro de Investigaciones Endocrinológicas “Dr. César Bergadá” (CEDIE) CONICET - FEI - División de Endocrinología, Hospital de Niños Ricardo Gutiérrez, Gallo 1330, Ciudad Autónoma de Buenos Aires, Argentina

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Maria Fernanda Riera Centro de Investigaciones Endocrinológicas “Dr. César Bergadá” (CEDIE) CONICET - FEI - División de Endocrinología, Hospital de Niños Ricardo Gutiérrez, Gallo 1330, Ciudad Autónoma de Buenos Aires, Argentina

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Silvina Beatriz Meroni Centro de Investigaciones Endocrinológicas “Dr. César Bergadá” (CEDIE) CONICET - FEI - División de Endocrinología, Hospital de Niños Ricardo Gutiérrez, Gallo 1330, Ciudad Autónoma de Buenos Aires, Argentina

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Maria Noel Galardo Centro de Investigaciones Endocrinológicas “Dr. César Bergadá” (CEDIE) CONICET - FEI - División de Endocrinología, Hospital de Niños Ricardo Gutiérrez, Gallo 1330, Ciudad Autónoma de Buenos Aires, Argentina

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In brief

FSH leads to glutamine dependence, which is required for mTORC1 activation and in consequence Sertoli cell proliferation.

Abstract

The spermatogenic capacity of adult individuals depends on, among other factors, the number of Sertoli cells (SCs) that result from the proliferative waves during development. FSH upregulates SC proliferation at least partly, through the activation of the PI3K/Akt/mTORC1 pathway, among other mechanisms. It is widely known that mTORC1 is a sensor of amino acids. Among amino acids, glutamine acquires relevance since it might contribute to cell cycle progression through the modulation of mTORC1 activity. It has not been studied yet whether glutamine intervenes in FSH-mediated regulation of SC proliferation and cell cycle progression, or if FSH has any effect on glutamine metabolism. Eight-day-old rat SCs were incubated in culture media without glutamine or with glutamine in the absence or presence of a glutamine transporter inhibitor or a glutaminase activity inhibitor under basal conditions or stimulated with FSH. The results obtained show that FSH does not promote SC proliferation and mTORC1 activation in the absence of glutamine. Also, FSH modulates glutamine metabolism increasing glutaminase isoform 2 and reducing glutamine synthetaseexpression. FSH did not promote SC proliferation and mTORC1 activation when glutaminase activity was inhibited. The results suggest that glutamine or its metabolites might cooperate with FSH in the upregulation of SC proliferation through mTORC1. In addition, as FSH modulates glutamine metabolism through the induction of glutaminase isoform 2, the hormonal control of glutamine metabolism might be part of the intricate signaling network triggered by FSH, which is crucial to establish the population of mature SCs that supports the reproductive function.

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Bogdan Doroftei Department of Mother and Child, Faculty of Medicine, University of Medicine and Pharmacy Grigore T. Popa, Iasi, Romania
Clinical Hospital of Obstetrics and Gynecology Cuza Voda, Iasi, Romania
Origyn Fertility Center, Iasi, Romania

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Ovidiu-Dumitru Ilie Department of Mother and Child, Faculty of Medicine, University of Medicine and Pharmacy Grigore T. Popa, Iasi, Romania

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Sergiu Timofeiov Department of Surgery, Faculty of Medicine, University of Medicine and Pharmacy Grigore T. Popa, Iasi, Romania
3rd Surgical Unit, St. Spiridon County Emergency Clinical Hospital, Iasi, Romania

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Ana-Maria Dabuleanu Clinical Hospital of Obstetrics and Gynecology Cuza Voda, Iasi, Romania
Origyn Fertility Center, Iasi, Romania

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Ioana-Sadyie Scripcariu Department of Mother and Child, Faculty of Medicine, University of Medicine and Pharmacy Grigore T. Popa, Iasi, Romania

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Romeo Micu Department of Human Assisted Reproduction of 1st Gynecology Clinic, University of Medicine and Pharmacy Iuliu Hatieganu, Cluj-Napoca, Romania

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Elena Tataranu Faculty of Medicine and Biological Sciences, Stefan cel Mare University of Suceava, Suceava, Romania

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In brief

Alpha-ketoglutarate is a common metabolite in the tricarboxylic acid cycle and is central in modulating the reproductive potential in animal models. The present scoping review systematically covers the spectrum of a wide range of evidence from different viewpoints, focusing on the underlying processes and mechanisms of the developmental framework, aiming to fill the gaps within the existing literature.

Abstract

Alpha-ketoglutarate is an important intermediate molecule in the tricarboxylic acid cycle with a prominent role in distinct biological processes such as cellular energy metabolism, epigenetic regulation, and signaling pathways. We conducted a registered scoping review (OSF: osf.io/b8nyt) to explore the impact of exogenous supplementation on reproductive capabilities. Our strategy included evaluating the main research literature from different databases like PubMed-MEDLINE, Web of ScienceTM, Scopus, and Excerpta Medica dataBASE using a specific systematic layout to encompass all investigations based on experimental models and critically compare the results. Twenty-one studies were included in the main body of this manuscript, which revealed that exogenous supplementation induced dose- and sex-dependent modifications. This metabolite modulates the expression of pluripotency genes, thus controlling stem cells’ self-renewal, differentiation, and reprogramming dynamics, while also alleviating structural transformations induced by exposure to heavy metals and other inhibitors. This significantly demonstrated a direct influence of alpha-ketoglutarate in mitigating oxidative stress and prolonging the lifespan, consequently supporting metabolic and endocrine adjustments. It influences oocyte quality and quantity, delays reproductive aging, and establishes an optimal competence framework for development with minimal risk of failure. Therefore, alpha-ketoglutarate is linked to improving reproductive performance, but further studies are needed due to a lack of studies on humans.

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Pérez-Gómez Alba Department of Animal Reproduction, INIA, CSIC, Madrid, Spain

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Flores-Borobia Inés Department of Animal Reproduction, INIA, CSIC, Madrid, Spain

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Hamze Julieta Gabriela Department of Animal Reproduction, INIA, CSIC, Madrid, Spain
Department of Cell Biology and Histology, Universidad de Murcia. International Excellence Campus for Higher Education and Research (Campus Mare Nostrum), Murcia, Spain

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Galiano-Cogolludo Beatriz Department of Animal Reproduction, INIA, CSIC, Madrid, Spain

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Lamas-Toranzo Ismael Department of Animal Reproduction, INIA, CSIC, Madrid, Spain

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González-Brusi Leopoldo Department of Animal Reproduction, INIA, CSIC, Madrid, Spain

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Ramos-Ibeas Priscila Department of Animal Reproduction, INIA, CSIC, Madrid, Spain

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Bermejo-Álvarez Pablo Department of Animal Reproduction, INIA, CSIC, Madrid, Spain

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In brief

Bovine embryos lacking SMC2 (a core component of condensins I and II) are unable to survive maternal recognition of pregnancy. SMC2 KO embryos are able to form blastocysts, exhibiting a reduced cell proliferation ability, and arrest their development shortly after hatching.

Abstract

Condensins are large protein complexes required for chromosome assembly and segregation during mitosis and meiosis. Mouse or bovine embryos lacking SMC2 (a core component of condensins I and II) do not complete development to term, but it is unknown when they arrest their development. Herein, we have assessed the developmental ability of bovine embryos lacking SMC2 due to a naturally occurring mutation termed HH3 (Holstein Haplotype 3) or by CRISPR-mediated gene ablation. To determine if embryos homozygous for the HH3 allele survive to maternal recognition of pregnancy, embryonic day (E)14 embryos were flushed from superovulated carrier cows inseminated with a carrier bull. Mendelian inheritance of the HH3 allele was observed at E14 conceptuses but conceptuses homozygous for HH3 failed to achieve elongation and lacked an embryonic disc. To assess the consequence of the ablation of condensins I and II at earlier developmental stages, SMC2 KO bovine embryos were generated in vitro using CRISPR technology. SMC2 KO embryos were able to form blastocysts but exhibited reduced cell proliferation as evidenced by a significantly lower number of total, trophectoderm (CDX2+), and inner cell mass (SOX2+) cells at Day (D) 8 post-fertilization compared to their WT counterparts and were unable to survive to D12 in vitro. SMC2 ablation did not alter relative telomere length at D8, D12, or E14. In conclusion, condensins I and II are required for blastomere mitosis during early development, and embryos lacking those complexes arrest their development shortly after blastocyst hatching.

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Ulrike Luderer U Luderer, Environmental and Occupational Health, University of California Irvine, Irvine, United States

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Particulate matter (PM) air pollution consists of liquid and solid particles, which are categorized by size as less than 10 (PM10) μm, 2.5 (PM2.5) μm, or 0.1μm (PM0.1 or ultrafine) in aerodynamic diameter and which vary in composition depending on the sources. PM exposure is ubiquitous and has been associated with many adverse health effects. This narrative review focuses on epidemiological and experimental studies that investigated the effects of PM exposure on female and male reproduction and on pregnancy.μ

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Takayuki Takahashi T Takahashi, Reproductive and Developmental Biology, Hokkaido University Faculty of Science Graduate School of Science, Sapporo, Japan

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Katsueki Ogiwara K Ogiwara, Reproductive and Developmental Biology, Hokkaido University Faculty of Science Graduate School of Science, Sapporo, 0600810, Japan

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Ovulation is the process by which a fertilizable oocyte is extruded from the interior of the follicle. Herein, we conducted a literature survey to explore the ovulation patterns of eleven sexually reproducing species belonging to 10 animal phyla. These results indicate a large variety of ovulation patterns. Further comparative biological and evolutionary considerations of these results led us to conclude that most female animals ovulate via follicle rupture. We propose that in all animals that ovulate by follicle rupture, two cellular events may be critically involved in the process: 1) the disintegration of cell junctional systems that lead to intracellular cytoskeleton rearrangement in the follicle cells and 2) the degradation of extracellular matrix (ECM) proteins filling between follicle cells. These events may result in follicular cell deformation and increased motility, both of which are necessary for the formation of a path through which oocytes escape from the follicle. In addition to the requirement of ECM degradation for disintegrating cell junctions, intensive ECM protein degradation at the apical region of the follicle probably became increasingly important in late-evolving animals, such as vertebrates, in which a thick follicle wall containing a large abundance of ECM proteins is formed. We also considered hypothetical scenarios for the evolution of ovulation in these animals. Furthermore, this article discusses the future problems that need to be solved for a more comprehensive understanding of ovulation in the animal kingdom.

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