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Fernando Correa Center for Pharmacological and Botanical Studies, National Research Council, School of Medicine

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Manuel L Wolfson Center for Pharmacological and Botanical Studies, National Research Council, School of Medicine

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Paula Valchi Center for Pharmacological and Botanical Studies, National Research Council, School of Medicine

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Julieta Aisemberg Center for Pharmacological and Botanical Studies, National Research Council, School of Medicine

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Ana María Franchi Center for Pharmacological and Botanical Studies, National Research Council, School of Medicine

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The endocannabinoid system (eCS), is a complex system, comprising the main endogenous ligands anandamide and 2-arachidonoyl glycerol, the cannabinoid receptors CB1 and CB2 and the biosynthetic and degrading enzymes. Cumulative evidence shows that the eCS plays an important role in reproduction, from egg fertilization to parturition. Therefore, alterations in this system, either by recreation/therapeutic use of cannabis or deregulation of the endogenous cannabinoids, might lead to adverse pregnancy outcomes, including retardation in embryo development, poor blastocyst implantation, inhibition of decidualization, miscarriage and compromised placentation. Nevertheless, the molecular mechanisms by which the eCS participates in different stages of pregnancy remain poorly understood. In this review, we will examine the evidence from animal and human studies to support the role of the eCS in implantation, early-to-late pregnancy and placentation as well as the difficulties of targeting this system for treatment of female infertility.

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Julieta Aylen Schander Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, CONICET-UBA, Buenos Aires, Argentina

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Julieta Aisemberg Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, CONICET-UBA, Buenos Aires, Argentina

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Fernando Correa Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, CONICET-UBA, Buenos Aires, Argentina

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Manuel Luis Wolfson Laboratorio de Fisiopatología de la Preñez y el Parto, Centro de Estudios Farmacológicos y Botánicos, CONICET-UBA, Buenos Aires, Argentina

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Lorena Juriol Laboratorio de Inmunología de la Reproducción, Centro de Estudios Farmacológicos y Botánicos, CONICET-UBA, Buenos Aires, Argentina

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Cora Cymeryng Laboratorio de Endocrinología Molecular, Centro de Estudios Farmacológicos y Botánicos, CONICET-UBA, Buenos Aires, Argentina

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Federico Jensen Laboratorio de Inmunología de la Reproducción, Centro de Estudios Farmacológicos y Botánicos, CONICET-UBA, 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, CONICET-UBA, Buenos Aires, Argentina

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Maternal lifestyle affects both mother health and pregnancy outcome in humans. Several studies have demonstrated that interventions oriented toward reducing stress and anxiety have positive effects on pregnancy complications such as preeclampsia, excessive gestational weight, gestational diabetes and preterm birth. In this work, we showed that the environmental enrichment (EE), defined as a noninvasive and biologically significant stimulus of the sensory pathway combined with voluntary physical activity, prevented preterm birth (PTB) rate by 40% in an inflammatory mouse model induced by the systemic administration of bacterial lipopolysaccharide (LPS). Furthermore, we found that EE modulates maternal metabolism and produces an anti-inflammatory environment that contributes to pregnancy maintenance. In pregnant mice uterus, EE reduces the expression of TLR4 and CD14 (the LPS receptor and its coactivator protein), preventing the LPS-induced increase in PGE2 and PGF2α release and nitric oxide synthase (NOS) activity. In cervical tissue, EE inhibits cervical ripening events, such as PGE2 release, matrix metalloproteinase (MMP)-9 increased activity and neutrophil recruitment, therefore conserving cervical function. It seems that EE exposure could mimic the stress and anxiety-reducing techniques mentioned above, explaining, at least partially, the beneficial effects of having a healthy lifestyle before and during gestation. Furthermore, we propose that designing an EE protocol for humans could be a noninvasive and preventive therapy for pregnancy complications, averting pre-term birth occurrence and dreaded sequelae that are present in the offspring born too soon.

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Fernando A Rivera School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA
School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA

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Luís G D Mendonça School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA

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Gláucio Lopes Jr School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA

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José E P Santos School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA

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Rolando V Perez School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA
School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA

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Marcel Amstalden School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA

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Abelardo Correa-Calderón School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA

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Ricardo C Chebel School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA
School of Veterinary Medicine, Department of Veterinary Population Medicine, Department of Animal Sciences, Department of Animal Science, Instituto de Ciencias Agrícolas, University of California Davis, Tulare, California 93274, USA

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Fertility of lactating dairy cows is associated with reduced progesterone (P4) concentration compared with nonlactating animals. The objective of the current study was to determine whether P4 during growth of the first follicular wave (FFW) affects embryo quality. Lactating Holstein cows at 33±3 days post partum were allocated to one of three treatments. Cows in the FFW and FFW with P4 (FFWP) treatments started the superstimulation protocol on day 1 of the estrous cycle and second follicular wave (SFW) cows started the superstimulation protocol on estrous cycle day 7. Cows were superstimulated with 400 mg of NIH-FSH-P1 (FSH) given twice daily for 5 days, two prostaglandin F (PGF) injections given with the ninth and tenth injections of FSH, GNRH given 48 h after the first PGF injection, and timed insemination 12 and 24 h after the GNRH injection. Cows in the FFWP treatment received two intravaginal P4 inserts during the superstimulation. Embryos were recovered 6.5 days after artificial insemination and excellent/good and fair embryos were frozen and transferred. Blood was sampled daily from estrous cycle day 0 until insemination from donor cows. During the superstimulation protocol, P4 was (P<0.01) greatest for SFW cows followed by FFWP and FFW cows respectively. The percentage of embryos–oocytes from SFW and FFWP cows classified as excellent/good and fair embryos was (P=0.02) greater than those of FFW cows. Pregnancy per embryo transfer was not (P≥0.73) affected by embryo donor treatment. Reduced embryo quality of cows induced to ovulate the follicles from the first follicular wave is a consequence of reduced P4 during follicle growth.

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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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