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Rui-Qi Chang R Chang, Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, China

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Jing-Cong Dai J Dai, Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, China

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Yu-Han Qiu Y Qiu, Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, China

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Yan Liang Y Liang, Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, China

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Xiao-Yu Hu X Hu, Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, China

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Ming-Qing Li M Li, Laboratory for Reproductive Immunology, Obstetrics and Gynecology Hospital of Fudan University, Shanghai, China

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Fan He F He, Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, China

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Decidual γδT (dγδT) cells help maintain maternal-fetal immunotolerance in early pregnancy. However, the mechanism underlying the accumulation of γδT cells in the decidua is unknown. Previous work showed that RANKL up-regulated intercellular adhesion molecule 1 (ICAM-1) in decidual stromal cells (DSCs) and Rankl knockout mice had limited dγδT cell populations. In this study, we measured the expression levels of RANKL/RANK and ICAM-1 in DSCs, in addition to the integrins of ICAM-1 on dγδT cells, and the quantity of dγδT cells from patients with recurrent spontaneous abortion (RSA) and normal pregnant women in the first trimester. RSA patients showed significantly decreased RANKL/RANK and ICAM-1/CD11a signaling in decidua, and a decreased percentage of dγδT cells, which was positively correlated with DSC-derived RANKL and ICAM-1. Next, in vitro adhesion experiment showed that the enhanced attraction of human DSCs to dγδT cells after RANKL over-expression was almost completely aborted by anti-ICAM-1. Furthermore, Rankl knockout mice showed a significant reduction in NF-κB activity compared with wild-type controls. Finally, we applied a selective NF-κB inhibitor named PDTC to validate the role of NF-κB in RANKL-mediated ICAM-1 up-regulation. Taken together, our data show that DSC-derived RANKL up-regulates ICAM-1 expression via the NF-κB pathway to enable γδT cell accumulation in the early decidua. A reduction in RANKL/ICAM-1 signaling in DSCs may result in insufficient accumulation of γδT cells in decidua and in turn, RSA.

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Noemi Monferini N Monferini, Department of Veterinary Medicine and Animal Sciences, University of Milan, Milano, Italy

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Pritha Dey P Dey, Department of Veterinary Medicine and Animal Sciences, University of Milan, Milano, Italy

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Ludovica Donadini L Donadini, Department of Veterinary Medicine and Animal Sciences, University of Milan, Milano, Italy

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Niki Katsakoglou N Katsakoglou, Department of Veterinary Medicine and Animal Sciences, University of Milan, Milano, Italy

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Federica Franciosi F Franciosi, Department of Veterinary Medicine and Animal Sciences, University of Milan, Milano, Italy

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Valentina Lodde V Lodde, Department of Veterinary Medicine and Animal Sciences, University of Milan, Milano, Italy

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Alberto Maria Luciano A Luciano, Department of Veterinary Medicine and Animal Sciences, University of Milan, Milano, Italy

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Primordial, primary, and secondary follicles (collectively defined as preantral follicles) constitute the most abundant source of gametes inside the mammalian ovarian cortex. The massive isolation of preantral follicles and the refinement of stage-specific protocols for in vitro follicle growth would provide a powerful tool to boost the rescue and restoration of fertility in assisted reproduction interventions in human medicine, animal breeding, and vulnerable species preservation. Nevertheless, together with an efficient culture system, the most significant limitation to implementing in vitro follicle growth is the lack of an efficient method to isolate viable and homogeneous sub-populations of primordial, primary, and secondary follicles suitable for in vitro culture. Our study provides a strategy for high-yielding mechanical isolation of primordial, primary, and early secondary follicles from a limited portion of the ovarian cortex in the bovine animal model.

In the first part of the study, we refined a mechanical isolation protocol of preantral follicles, adopting specific methodological strategies to separate viable and distinct sub-populations of primordial (oblate and prolate forms), primary, and early secondary follicles from 0.16 cm3 of the ovarian cortex. In the second part of the study, we tested the effectiveness of the isolation protocol, considering the individual's age as a critical factor, bearing in mind the progressive decrease in the ovarian reserve that naturally accompanies the reproductive lifespan.

Our study provides a way for designing quantitative and conservative fertility preservation approaches to preserve organ function and minimize the invasiveness of the interventions, also considering age-related differences.

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João Vitor Alcantara da Silva Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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Jessica Ispada Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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Ricardo Perecin Nociti Department of Veterinary Medicine, Faculty of Animal Sciences and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil

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Aldcejam Martins da Fonseca Junior Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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Camila Bruna de Lima Département des Sciences Animales, Laval University, Canada

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Erika Cristina dos Santos Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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Marcos Roberto Chiaratti Department of Genetics and Evolution, Federal University of Sao Carlos, Sao Carlos, SP, Brazil

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Marcella Pecora Milazzotto Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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In brief

Pyruvate metabolism is one of the main metabolic pathways during oocyte maturation. This study demonstrates that pyruvate metabolism also regulates the epigenetic and molecular maturation in bovine oocytes.

Abstract

Pyruvate, the final product of glycolysis, undergoes conversion into acetyl-CoA within the mitochondria of oocytes, serving as a primary fuel source for the tricarboxylic acid (TCA) cycle. The citrate generated in the TCA cycle can be transported to the cytoplasm and converted back into acetyl-CoA. This acetyl-CoA can either fuel lipid synthesis or act as a substrate for histone acetylation. This study aimed to investigate how pyruvate metabolism influences lysine 9 histone 3 acetylation (H3K9ac) dynamics and RNA transcription in bovine oocytes during in vitro maturation (IVM). Bovine cumulus–oocyte complexes were cultured in vitro for 24 h, considering three experimental groups: Control (IVM medium only), DCA (IVM supplemented with sodium dichloroacetate, a stimulant of pyruvate oxidation into acetyl-CoA), or IA (IVM supplemented with sodium iodoacetate, a glycolysis inhibitor). The results revealed significant alterations in oocyte metabolism in both treatments, promoting the utilization of lipids as an energy source. These changes during IVM affected the dynamics of H3K9ac, subsequently influencing the oocyte's transcriptional activity. In the DCA and IA groups, a total of 148 and 356 differentially expressed genes were identified, respectively, compared to the control group. These findings suggest that modifications in pyruvate metabolism trigger the activation of metabolic pathways, particularly lipid metabolism, changing acetyl-CoA availability and H3K9ac levels, ultimately impacting the mRNA content of in vitro matured bovine oocytes.

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Chad S Driscoll Department of Animal Science, Developmental Epigenetics Laboratory, Reproductive and Developmental Sciences Program, Michigan State University, East Lansing, Michigan, USA

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Jaehwan Kim Department of Animal Science, Developmental Epigenetics Laboratory, Reproductive and Developmental Sciences Program, Michigan State University, East Lansing, Michigan, USA
Department of Animal Sciences, University of Missouri, Columbia, Missouri, USA

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Mohamed Ashry Department of Animal Science, Developmental Epigenetics Laboratory, Reproductive and Developmental Sciences Program, Michigan State University, East Lansing, Michigan, USA

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Jason G Knott Department of Animal Science, Developmental Epigenetics Laboratory, Reproductive and Developmental Sciences Program, Michigan State University, East Lansing, Michigan, USA

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Transcription factor AP2 gamma (TFAP2C) is a well-established regulator of the trophoblast lineage in mice and humans, but a handful of studies indicate that TFAP2C may play an important role in pluripotency. Here, we hypothesize and provide new evidence that TFAP2C functions as an activator of trophoblast and pluripotency genes during preimplantation embryo development.

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Carolina Marvaldi Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, Universidad de Buenos Aires-Consejo Nacional de Investigaciones en Ciencia y Técnica, Ciudad Autónoma de Buenos Aires, Argentina

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Felisa Herrero Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, Universidad de Buenos Aires-Consejo Nacional de Investigaciones en Ciencia y Técnica, Ciudad Autónoma de Buenos Aires, Argentina

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Clare Johnson Department of Psychological and Brain Sciences, Indiana University, Bloomington, Indiana, USA

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Julieta Aylen Schander Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, Universidad de Buenos Aires-Consejo Nacional de Investigaciones en Ciencia y Técnica, Ciudad Autónoma de Buenos Aires, Argentina

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Fernando Correa Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, Universidad de Buenos Aires-Consejo Nacional de Investigaciones en Ciencia y Técnica, Ciudad Autónoma de Buenos Aires, Argentina

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Maximiliano Cella Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, Universidad de Buenos Aires-Consejo Nacional de Investigaciones en Ciencia y Técnica, Ciudad Autónoma de Buenos Aires, Argentina

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Julieta Aisemberg Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, Universidad de Buenos Aires-Consejo Nacional de Investigaciones en Ciencia y Técnica, Ciudad Autónoma de Buenos Aires, Argentina

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Ana María Franchi Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, Universidad de Buenos Aires-Consejo Nacional de Investigaciones en Ciencia y Técnica, Ciudad Autónoma de Buenos Aires, Argentina

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Heather Bradshaw Department of Psychological and Brain Sciences, Indiana University, Bloomington, Indiana, USA

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Manuel Luis Wolfson Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, Universidad de Buenos Aires-Consejo Nacional de Investigaciones en Ciencia y Técnica, Ciudad Autónoma de Buenos Aires, Argentina

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In brief

The cervix plays a crucial role not only in the maintenance of pregnancy but also during delivery, when it undergoes extensive changes. This study highlights the involvement of the endocannabinoidome in cervical remodeling, emphasizing its relevance in the shift from a nonpregnant to pregnant state and its potential contribution to preterm delivery in inflammatory contexts.

Abstract

During pregnancy, the main role of the cervix is to isolate the fetus from outside pathogens and maintain the relatively closed system of uterine gestation. Conversely, toward the end of pregnancy, the cervix must be remodeled to increase flexibility and allow the delivery. This process is called cervical remodeling and dysregulation of the process plays a role in premature delivery. The endocannabinoidome plays an important role in several reproductive events; however, its function on cervical tissue throughout pregnancy is poorly understood. The goal of this study was to evaluate the presence and participation of the endocannabinoidome in lipopolysaccharide (LPS)-induced cervical changes. Therefore, we evaluated key components of the endocannabinoidome in cervical tissue from nonpregnant mice and pregnant mice with and without LPS treatment. Using mass spectrometric analysis, we found an increase in anandamide and 2-arachidonoylglycerol in the cervix of pregnant mice when compared to nonpregnant mice. We have also found a reduction in FAAH protein expression in these tissues. Furthermore, when treated with LPS, we observed a reduction in the cervical immunostaining with anti-CB1 and anti-CB2 antibodies. Likewise, using cervix explants from pregnant mice, we found that LPS significantly increased cervical metalloprotease activity and cyclooxygenase 2, which were subsequently modulated by cannabinoid receptor antagonists. Collectively, our findings suggest that an LPS-induced imbalance of cervix endocannabinoidome likely contributes to premature cervical remodeling, which is part of the key components that contribute to premature delivery.

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Giorgia Podico G Podico, Veterinary Clinical Medicine, University of Illinois at Urbana-Champaign, Urbana, United States

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João H. Bittar J Bittar, Large Animal Clinical Sciences, University of Florida, Gainesville, United States

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Shavahn C Loux S Loux, Department of Veterinary Science , University of Kentucky Maxwell H Gluck Equine Research Center, Lexington, United States

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Fabiana F. Souza F Souza, Department of Veterinary Surgery and Reproduction, Sao Paulo State University, Botucatu, Brazil

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Igor F Canisso I Canisso, Department of Veterinary Clinical Medicine, University of Illinois Urbana-Champaign, Urbana, United States

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Anecdotal experience suggests horse mares have less post-breeding inflammation and better fertility when bred with donkeys. This study aimed to compare the post-breeding inflammatory response of mares exposed to donkey and horse semen and seminal plasma and evaluate the proteome and metabolome of donkey and horse sperm and seminal plasma. Uterine edema, intrauterine fluid accumulation, PMNs on cytology, and concentrations of progesterone, and pro- and anti-inflammatory cytokines (IL1, IL1, IL4, IL6, CXCL8, IL10) concentrations were assessed pre-and post-infusion of semen and seminal plasma (donkey and horse). The metabolome and proteome were analyzed by LC-MS/MS. Mare cycles bred with horse semen had a greater progesterone concentration than those cycles bred with donkey semen at 8 days post-ovulation (P=0.046). At 6 h post-infusion, the inflammatory response due to the donkey semen tended to be lower (P=0.074). Donkey seminal plasma had anti-inflammatory properties compared to horse semen and seminal plasma, as determined by fewer neutrophils on uterine cytology (P<0.05). Horse semen induced resulted in a greater concentrations of IL6 and lesser concentrations of IL1 (P<0.05). Concentrations of PGE1, PGE3, and lactoferrin PGE1, PGE3, and lactoferrin concentrations were significantly more abundant in donkey sperm and seminal plasma. Prostaglandins play an important role in immunomodulation and might contribute to the response triggered in inter-species breeding. In conclusion, breeding horse mares with donkey semen induces a similar post-breeding endometritis to horse semen. Donkey seminal plasma results in a lower post-infusion inflammatory response than other combinations in the immediate post-breeding.

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Uma Shinde Neuroendocrinology, ICMR-National Institute for Research in Reproductive & Child Health, Parel, Mumbai, Maharashtra, India

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Aishwarya Rao Innate Immunity, ICMR-National Institute for Research in Reproductive & Child Health, Parel, Mumbai, Maharashtra, India

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Vandana Bansal Department of Obstetrics and Gynaecology, Nowrosjee Wadia Maternity Hospital, Parel, Mumbai, Maharashtra, India

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Dhanjit Kumar Das Stem Cell Biology, ICMR-National Institute for Research in Reproductive & Child Health, Parel, Mumbai, Maharashtra, India

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Nafisa Huseni Balasinor Neuroendocrinology, ICMR-National Institute for Research in Reproductive & Child Health, Parel, Mumbai, Maharashtra, India

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Taruna Madan Innate Immunity, ICMR-National Institute for Research in Reproductive & Child Health, Parel, Mumbai, Maharashtra, India

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In brief

Circulating extracellular vesicles of placental/amniochorionic origin carry placental/amniochorionic proteins and nucleic acids with the potential to facilitate non-invasive diagnosis of pregnancy-related disorders. The study reports an improvised method for the enriched isolation of extracellular vesicles of placental/amniochorionic origin using the two markers, PLAP and HLA-G.

Abstract

Extracellular vesicles (EVs) are membrane-bound nanovesicles secreted from the cells into extracellular space and body fluids. They are considered ‘fingerprints of parent cells’, which can reflect their physiological and functional states. During pregnancy, EVs are produced by the syncytiotrophoblasts and extravillous trophoblasts and are released into the maternal bloodstream. In the present study, placental alkaline phosphatase (PLAP)-specific extracellular vesicles were isolated from maternal serum-derived EVs (SDE) across pregnancy. Transmission electron microscopy and dynamic light scattering analysis showed that the isolated EVs exhibited a spherical morphology with ~30–150 nm size range. Nanoparticle tracking analysis indicated that the concentration of PLAP+ serum-derived EVs (PLAP+-SDE) increased across the gestation. PLAP+-SDE contained DNA with LINE1 promoter methylation pattern. C19 miRNA cluster miRNAs (miR 515-5p, 519e and 520f) were present in PLAP+-SDE along with other miRNAs (miR-133-3p, miR210-3p and miR-223-3p). PLAP+-SDE confirmed the presence of EV markers (CD63 and CD9), along with placental proteins (PLAP and cullin 7). A modified novel strategy to extract an enriched population of circulating placental/amniochorionic EVs was devised employing an additional marker of extravillous trophoblasts, human leukocyte antigen G (HLA-G), along with PLAP. The isolated pooled placental/amniochorionic (PLAP+&HLA-G+) serum-derived EVs (PP-SDE) showed ~two-fold increased protein levels of HLA-G in the third-trimester pregnant women compared to the non-pregnant controls. Future studies will be focused on validation of this novel strategy to isolate an enriched population of placental/amniochorionic EVs to facilitate a better understanding of placental physiology and pathophysiology.

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Emma G Whatley E Whatley, BioSciences, The University of Melbourne, Parkville, Australia

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Alexandra J Harvey A Harvey, Biosciences, The University of Melbourne, Parkville, Australia

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David K Gardner D Gardner, BioSciences, The University of Melbourne, Parkville, Australia

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A ketogenic diet elevates blood β-hydroxybutyrate to concentrations that perturb the development, metabolism, histone acetylation (H3K27ac) and viability of preimplantation mouse embryos in vitro. However, whether a ketogenic diet alters β-hydroxybutyrate concentrations within female reproductive fluid is unknown. This study aimed to quantify glucose and β-hydroxybutyrate within mouse blood and oviduct fluid following standard diet and ketogenic diet consumption and to assess whether a maternal periconceptional ketogenic diet impacts in vivo embryo development and blastocyst H3K27ac. Female C57BL/6 x CBA mice were fed a standard or ketogenic diet (n=24 each) for 24-27 days. Glucose and β-hydroxybutyrate were quantified in blood via an electronic monitoring system, and in oviduct fluid via ultramicrofluorescence. The developmental grade of flushed blastocysts was recorded, and blastocyst cell number and H3K27ac was assessed via immunofluorescence. A maternal ketogenic diet elevated β-hydroxybutyrate in day 24 blood (P<0.001) and oviduct fluid (P<0.05) compared with a standard diet, whereas glucose was unchanged. A periconceptional ketogenic diet did not impact blastocyst cell number, however, significantly delayed blastocyst development (P<0.05) and reduced trophectoderm-specific H3K27ac (P<0.05) compared with standard diet-derived embryos. Maternal ketogenic diet consumption is therefore associated with reproductive tract nutrient changes and altered embryonic development and epigenetics in vivo. Future studies to assess whether periconceptional/gestational ketogenic diet consumption impacts human preimplantation, fetal, and long-term offspring development and health are warranted.

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Isabella G Cossu Department of Biomedical Sciences, University of Pennsylvania School of Veterinary Medicine, Philadelphia, Pennsylvania, USA

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N Adrian Leu Department of Biomedical Sciences, University of Pennsylvania School of Veterinary Medicine, Philadelphia, Pennsylvania, USA

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Yongjuan Guan Department of Biomedical Sciences, University of Pennsylvania School of Veterinary Medicine, Philadelphia, Pennsylvania, USA
College of Life Sciences, Capital Normal University, Beijing, China

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P Jeremy Wang Department of Biomedical Sciences, University of Pennsylvania School of Veterinary Medicine, Philadelphia, Pennsylvania, USA

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In brief

The dissociation of HORMA domain protein 2 (HORMAD2) from the synaptonemal complex is tightly regulated. This study reveals that the N-terminal region of HORMAD2 is critical for its dissociation from synapsed meiotic chromosomes.

Abstract

During meiosis, homologous chromosomes undergo synapsis and recombination. HORMA domain proteins regulate key processes in meiosis. Mammalian HORMAD1 and HORMAD2 localize to unsynapsed chromosome axes but are removed upon synapsis by the TRIP13 AAA+ ATPase. TRIP13 engages the N-terminal region of HORMA domain proteins to induce an open conformation, resulting in the disassembly of protein complexes. Here, we report introduction of a 3×FLAG-HA tag to the N-terminus of HORMAD2 in mice. Coimmunoprecipitation coupled with mass spectrometry identified HORMAD1 and SYCP2 as HORMAD2-associated proteins in the testis. Unexpectedly, the N-terminal tagging of HORMAD2 resulted in its abnormal persistence along synapsed regions in pachynema and ectopic localization to telomeres in diplonema. Super-resolution microscopy revealed that 3×FLAG-HA-HORMAD2 was distributed along the central region of the synaptonemal complex, whereas wild-type HORMAD1 persisted along the lateral elements in 3×FLAG-HA-HORMAD2 meiocytes. Although homozygous mice completed meiosis and were fertile, homozygous males exhibited a significant reduction in sperm count. Collectively, these results suggest that the N-terminus of HORMAD2 is important for its timely removal from meiotic chromosome axes.

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Zoe M G Skalkos The University of Sydney, School of Life and Environmental Sciences, Sydney, NSW, Australia

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James U Van Dyke La Trobe University, Department of Environment and Genetics, School of Agriculture, Biomedicine and Environment, Wodonga, VIC, Australia

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Samson N Dowland The University of Sydney, School of Medical Sciences, Sydney, NSW, Australia

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Camilla M Whittington The University of Sydney, School of Life and Environmental Sciences, Sydney, NSW, Australia

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In brief

Seahorses exhibit male pregnancy and are thus valuable comparative models for the study of the physiology and evolution of pregnancy. This study shows that protein is transported from fathers to developing embryos during gestation, and provides new knowledge about paternal contributions to embryonic development.

Abstract

Syngnathid embryos (seahorses, pipefishes and seadragons) develop on or in the male in a specialised brooding structure (brood pouch). Seahorse brood pouches supply nutrients, including lipids, to developing embryos (patrotrophy). We tested the hypothesis that proteins, vital for gene regulation and tissue growth during embryogenesis, are also transported from father to embryos, using the Australian pot-bellied seahorse, Hippocampus abdominalis. We used dry masses and total nitrogen content to estimate the total protein content of newly fertilised egg and neonate H. abdominalis. Neonates contained significantly greater protein mass than newly fertilised eggs. This result indicates that paternal protein transport to developing embryos occurs during H. abdominalis pregnancy. This study is the first to show paternal protein transport during pregnancy in seahorses, and furthers our understanding of paternal influence on embryonic development in male pregnant vertebrates.

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