Transient estrogen exposure from birth affects uterine expression of developmental markers in neonatal gilts with lasting consequences in pregnant adults

Chen, Joseph C.; Wiley, Anne A.; Ho, Teh Yuan; Frankshun, Amy Lynn; Hord, Kristin M.; Bartol, Frank F.; Bagnell, Carol A.

doi:10.1530/rep-09-0454

Cited by 26 publications

(24 citation statements)

References 40 publications

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“…Neonatal porcine uterine development is both ESR1 dependent and estrogen sensitive (Bartol et al 1993, Tarleton et al 1999, 2003, Chen et al 2010. Therefore, it was important to determine the extent to which uterine ESR1 expression might be regulated via a lactocrine mechanism.…”

Section: Discussionmentioning

confidence: 99%

“…Between birth and PND 3, the porcine endometrium undergoes an important morphogenetic transition, as glandular epithelium differentiates from luminal epithelium and nascent uterine glands begin to penetrate underlying stroma (Masters et al 2007). These events are both ER dependent and estrogen sensitive (Bartol et al 1993, Tarleton et al 1999, 2003, Chen et al 2010. Data support the idea that factors affecting patterns of porcine uterine ESR1 expression and ER activation during early postnatal life define both the developmental program and trajectory of developing uterine tissues with lasting consequences in adults.…”

Section: Introductionmentioning

confidence: 92%

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Milk-borne lactocrine-acting factors affect gene expression patterns in the developing neonatal porcine uterus

Chen¹,

Frankshun²,

Wiley³

et al. 2011

Reproduction

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Lactocrine communication of milk-borne bioactive factors (MbFs) from mother to offspring through nursing can affect neonatal development with lasting consequences. Relaxin (RLX), a lactocrine-active peptide found in porcine colostrum, stimulates estrogen receptor-a (ESR1) expression required for uterine development shortly after birth (postnatal dayZPND 0). Whether other MbFs or cooperative lactocrine mechanisms affect the neonatal uterine developmental program is unknown. To determine the effects of age, nursing, and exogenous RLX on gene expression associated with uterine development, gilts (nZ4-5/group) were assigned to nurse ad libitum or to receive milk replacer, with or without exogenous RLX (20 mg/kg BW i.m./6 h for 48 h), from birth to PND 2 when uteri were collected. Body weight and uterine weight increased (P!0.05) similarly from birth to PND 2 in all gilts. However, colostrum consumption was required for normal uterine ESR1, vascular endothelial growth factor (VEGFA), matrix metalloproteinase 9 (MMP9), and RLX receptor (RXFP1) protein and/or transcript expression on PND 2. Uterine ESR1, VEGFA, and MMP9 protein levels were below (P!0.01) the assay sensitivity in replacer-fed gilts. Supplemental RLX increased (P!0.05) uterine ESR1 protein and mRNA in nursed gilts, as well as VEGFA protein in nursed and VEGFA mRNA in both nursed and replacer-fed gilts. RLX treatment did not affect uterine MMP9 mRNA levels. When compared with replacer-fed gilts on PND 2, uterine RXFP1 mRNA was reduced (P!0.05) in nursed gilts and in RLX-supplemented replacer-fed gilts. These results constitute the first evidence that establishment of the neonatal porcine uterine developmental program requires maternal lactocrine support.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 92%

Milk-borne lactocrine-acting factors affect gene expression patterns in the developing neonatal porcine uterus

Chen¹,

Frankshun²,

Wiley³

et al. 2011

Reproduction

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“…There are no available published data that reported the expression of VEGF in the bitch uterus during pregnancy, although there are some information about the expression of this gene in other species of mammals, including pigs, rodents and human (Douglas et al 2009, Kaczmarek et al 2009, Kalkunte et al 2009, Bolat et al 2010, Chen et al 2010, Souza et al 2010. It was previously clearly demonstrated that the activation of VEGF-related biochemical pathway induces the processes of proper angiogenesis and vascularization.…”

Section: Discussionmentioning

confidence: 99%

Analysis of integrins and vascular endothelial growth factor isoforms mRNA expression in the canine uterus during perimplantation period

Bukowska¹,

Kempisty²,

Jackowska³

et al. 2011

Polish Journal of Veterinary Sciences

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Integrins are the major receptors within the extracellular matrix (ECM) that mediate several functions connected with cell life and metabolism, such as cell adhesion, migration, cytoskeletal organization, proliferation, survival, and differentiation. A vascular endothelial growth factor (VEGF) is one of the most important angiogenic factors. It has been suggested that the expression of this gene may play crucial physiological roles in reproductive organs.All investigated endometrial tissues were isolated on day 10-12 after mating. Control bitches, used in this study, were in metestrus, which was determined according to the vaginal cytology and progesterone level in blood. Early pregnancy was verified by flushing the uterine horns with PBS. Total RNA was isolated from the bitches endometrium by means of the Chomczyński and Sacchi method, treated by DNase I, and reverse-transcribed into cDNA. A quantitative analysis of integrins α2b, β2 and β3, VEGF 164, 182 and 188 cDNA was performed by RT-PCR.In results we have shown an increased expression of all investigated genes (integrins α2b, β2 and β3, VEGF 164, 182, and 188) in pregnant bitches uterus as compared to non-pregnant females (P<0.001).Our results indicated that the expression of genes encoding integrins and vascular endothelial growth factors is different in relation to the time of the embryo implantation and it is increased in the first period of this process. This may be associated with the induction of specific mechanisms responsible for receptivity of uterus following the embryo attachment. In addition, all of investigated genes are up-regulated in a pregnancy-specific manner and the increased expression of these genes may regulate the uterus function during the implantation of canine embryos.

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“…HOXA10 has been shown to be essential not only for uterine development, but also for implantation [8]. This gene has been shown to be expressed in adult murine [9], canine [10], primate [11], human [8, 9], and more recently porcine [12,13] uteri. In pigs, HOXA10 protein was localized in the luminal and glandular epithelium, stroma and blood vessels of the endometrium, but also in the myometrium of the uterus [13].…”

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confidence: 99%

“…However, the majority of embryos commence implantation but are resorbed early in the post-implantation period [14]. Moreover, HOXA10 expression is regulated by P4 and/or E2 in human [8] Recently, E2-stimulated expression of HOXA10 gene was observed in uteri of postnatal day 14 piglets [12].Prostaglandins (PGs) produced by the uterus play an essential role in regulation of the estrous cycle and during maternal recognition of pregnancy in many species, including the pig [4,18]. The rate-limiting enzyme in PG production is prostaglandin H synthase (PGHS; also known as cyclooxygenase), which catalyzes the conversion of arachidonic acid to PGH2 [19], the common substrate for various PGs.…”

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confidence: 99%

Effect of Steroids on HOXA10 mRNA and Protein Expression and Prostaglandin Production in the Porcine Endometrium

Blitek

Kiewisz

Wacławik

et al. 2010

Journal of Reproduction and Development

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Abstract. The homeobox A (HOXA) family of genes is responsible for segmental development of the female reproductive tract during embryogenesis. However, HOXA10 has been shown to be essential not only for uterus development, but also for implantation. Persistent expression and steroid-dependent regulation of this gene has been demonstrated in adult human, primate, murine and canine uteri. Moreover, HOXA10-dependent expression of prostaglandin H synthase-2 (PGHS-2), a key enzyme in prostaglandin production, has been previously detected. The role of the HOXA10 gene in the porcine uterus is not well established. Therefore, the present studies were undertaken to 1) examine the effect of E2 and P4 on HOXA10 mRNA and protein content in the endometrium collected on day 9 of the estrous cycle and 2) determine the PGHS-2 protein expression and PGE2 and PGF2α secretion from endometrial tissue in response to steroid treatment. Endometrial explants collected from mature gilts on day 9 of the estrous cycle were incubated with E2 (1-100 nM), P4 (10-1000 nM) or E2 (10 nM) and P4 (100 nM) for 24 h. E2 alone or E2 in the presence of P4 increased HOXA10 mRNA expression in the endometrium (P<0.05). The HOXA10 protein level was upregulated in response to E2, P4 and both steroids administered simultaneously (P<0.05). Moreover, E2 and P4 stimulated PGHS-2 protein expression in cultured endometrial explants. PGE2, but not PGF2α, secretion increased in the presence of E2 (P<0.05). However, the release of both prostaglandins was decreased after treatment of endometrial explants with the highest dose of P4 (P<0.01). These results demonstrate that E2 and P4 are important regulators of HOXA10 gene expression in the adult porcine endometrium during the mid-luteal phase of the estrous cycle. Additionally, the similar profiles of endometrial HOXA10 and PGHS-2 expression in the presence of E2 and P4 indicate that both genes are simultaneously regulated by steroids in the porcine uterus. Key words: Endometrium, Estradiol, HOXA10, PGHS-2, Pig, Progesterone, Prostaglandins (J. Reprod. Dev. 56: [643][644][645][646][647][648] 2010) he uterine endometrium is one of the most dynamic tissues in the organism, undergoing morphological and physiological changes during each estrous cycle. Disorders in endometrial development may lead to lack of or improper implantation, pregnancy failure or infertility. Among the different hormones, estradiol (E2) and progesterone (P4) of ovarian origin are crucial regulators of endometrial receptivity and embryo-maternal cross-talk in many species [1][2][3][4]. It is obvious that the action of P4 in priming the uterus is absolutely essential to attain uterine receptivity for implantation, but the requirement of E2 of ovarian origin is speciesspecific [1]. However, the molecular mechanisms that direct the ordered proliferation, differentiation and cell death associated with the normal menstrual or estrous cycles are still not well characterized. Good candidates for regulation of gene expression in the endometrium are ho...

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Transient estrogen exposure from birth affects uterine expression of developmental markers in neonatal gilts with lasting consequences in pregnant adults

Cited by 26 publications

References 40 publications

Milk-borne lactocrine-acting factors affect gene expression patterns in the developing neonatal porcine uterus

Milk-borne lactocrine-acting factors affect gene expression patterns in the developing neonatal porcine uterus

Analysis of integrins and vascular endothelial growth factor isoforms mRNA expression in the canine uterus during perimplantation period

Effect of Steroids on HOXA10 mRNA and Protein Expression and Prostaglandin Production in the Porcine Endometrium

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