Neonatal exposure to progesterone and estradiol alters uterine morphology and luminal protein content in adult beef heifers

Bartol, F.F.; Johnson, L. W.; Floyd, James G.; Wiley, Anne A.; Spencer, Thomas E.; Buxton, Donald F.; Coleman, D.A.

doi:10.1016/0093-691x(95)00035-7

Cited by 39 publications

(34 citation statements)

References 28 publications

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“…Morphologically normal blastocysts are present in uterine flushes of bred UGKO ewes on days 6 and 9 post-mating, but not on day 14 (Gray et al 2001b(Gray et al , 2002 when uteri contain either no conceptus or a severely growth-retarded tubular conceptus. Similarly, exposure of neonatal heifers to progestins alters uterine development and reduces pregnancy success in adult cows (Bartol et al 1995). These results demonstrate that histotroph from endometrial epithelia are required for peri-implantation blastocyst survival and elongation in sheep and likely cattle.…”

Section: Proteomics and Metabolomicsmentioning

confidence: 72%

Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches

Spencer¹,

Sandra²,

Wolf³

2008

Reproduction

270

253

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This review summarizes new knowledge on expression of genes and provides insights into approaches for study of conceptus-endometrial interactions in ruminants with emphasis on the peri-implantation stage of pregnancy. Conceptus-endometrial interactions in ruminants are complex and involve carefully orchestrated temporal and spatial alterations in gene expression regulated by hormones from the ovary and conceptus. Progesterone is the hormone of pregnancy and acts on the uterus to stimulate blastocyst survival, growth, and development. Inadequate progesterone levels or a delayed rise in progesterone is associated with pregnancy loss. The mononuclear trophectoderm cells of the elongating blastocyst synthesize and secrete interferon-t (IFNT), the pregnancy recognition signal. Trophoblast giant binucleate cells begin to differentiate and produce hormones including chorionic somatomammotropin 1 (CSH1 or placental lactogen). A number of genes, induced or stimulated by progesterone, IFNT, and/or CSH1 in a cell-specific manner, are implicated in trophectoderm adhesion to the endometrial luminal epithelium and regulation of conceptus growth and differentiation. Transcriptional profiling experiments are beginning to unravel the complex dynamics of conceptus-endometrial interactions in cattle and sheep. Future experiments should incorporate physiological models of pregnancy loss and be complemented by metabolomic studies of uterine lumen contents to more completely define factors required for blastocyst survival, growth, and implantation. Both reduction and holistic approaches will be important to understand the multifactorial phenomenon of recurrent pregnancy loss and provide a basis for new strategies to improve pregnancy outcome and reproductive efficiency in cattle and other domestic animals.

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Section: Proteomics and Metabolomicsmentioning

confidence: 72%

Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches

Spencer¹,

Sandra²,

Wolf³

2008

Reproduction

270

253

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“…Results of the present study indicate that Nor exposure limited to 8 weeks from birth is sufficient to induce the UGKO phenotype. However, transient neonatal exposure to endocrine disrupters of development can permanently alter patterns of uterine gene expression and responses to steroid hormones, as shown in the mouse [20][21], cow [12,22], pig [23], and sheep [9]. Bartol et al [14] found aberrantly formed, nascent endometrial glands in uteri on PND 26 in ewes exposed to Nor from birth to PND 13 [14].…”

Section: Discussionmentioning

confidence: 99%

Ovine Uterine Gland Knock-Out Model: Effects of Gland Ablation on the Estrous Cycle1

Gray

Bartol

Taylor

et al. 2000

Biology of Reproduction

108

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Ovine endometrial gland development is a postnatal event that can be inhibited epigenetically by chronic exposure of ewe lambs to a synthetic progestin from birth to puberty. As adults, these neonatally progestin-treated ewes lack endometrial glands and display a uterine gland knockout (UGKO) phenotype that is useful as a model for study of endometrial function. Here, objectives were to determine: 1) length of progestin exposure necessary from birth to produce the UGKO phenotype in ewes; 2) if UGKO ewes display normal estrous cycles; and 3) if UGKO ewes could establish and/or maintain pregnancy. Ewe lambs (n = 22) received a Norgestomet (Nor) implant at birth and every two weeks thereafter for 8 (Group I), 16 (Group II), or 32 (Groups III and IV) weeks. Control ewe lambs (n = 13) received no Nor treatment (Groups V and VI). Ewes in Groups I, II, III, and VI were hemihysterectomized (Hhx) at 16 weeks of age. After puberty, the remaining uterine horn in Hhx ewes was removed on either Day 9 or 15 of the estrous cycle (Day 0 = estrus). Histological analyses of uteri indicated that progestin exposure for 8, 16, or 32 weeks prevented endometrial adenogenesis and produced the UGKO phenotype in adult ewes. Three endometrial phenotypes were consistently observed in Nor-treated ewes: 1) no glands, 2) slight glandular invaginations into the stroma, and 3) limited numbers of cyst- or gland-like structures in the stroma. Overall patterns of uterine progesterone, estrogen, and oxytocin receptor expression were not different in uteri from adult cyclic control and UGKO ewes. However, receptor expression was variegated in the ruffled luminal epithelium of uteri from UGKO ewes. Intact UGKO ewes displayed altered estrous cycles with interestrous intervals of 17 to 43 days, and they responded to exogenous prostaglandin F(2 approximately ) (PGF) with luteolysis and behavioral estrus. During the estrous cycle, plasma concentrations of progesterone in intact control and UGKO ewes were not different during metestrus and diestrus, but levels did not decline in many UGKO ewes during late diestrus. Peak peripheral plasma concentrations of PGF metabolite, in response to an oxytocin challenge on Day 15, were threefold lower in UGKO compared to control ewes. Intact UGKO ewes bred repeatedly to intact rams did not display evidence of pregnancy based on results of ultrasound. Collectively, results indicate that 1) transient, progestin-induced disruption of ovine uterine development from birth alters both structural and functional integrity of the adult endometrium; 2) normal adult endometrial integrity, including uterine glands, is required to insure a luteolytic pattern of PGF production; and 3) the UGKO phenotype, characterized by the absence of endometrial glands and a compact, disorganized endometrial stroma, limits or inhibits the capacity of uterine tissues to support the establishment and/or maintenance of pregnancy.

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“…All primers were designed using Primer Express Software (Applied Biosystems, Foster City, CA) and manufactured by Eurofins MWG (Ebersberg, Germany; Supplementary Table S1). 1 All reactions were performed using 50 ng of cDNA, 10 l of SYBR Green master mix (Applied Biosystems), and primers at a concentration of 300 nM each. Two transcript variants exist for LGALS9, due to the deletion of a coding exon, resulting in transcript variant 1 (long isoform), which codes for the entire length of 355 amino acids, and transcript variant 2 (short isoform), which lacks 32 amino acids (aa149 -aa180), both of which were analyzed by Q-RT-PCR.…”

Section: Animal Model and Tissue Collectionmentioning

confidence: 99%

Endometrial expression of progesterone-induced blocking factor and galectins-1, -3, -9, and -3 binding protein in the luteal phase and early pregnancy in cattle

Okumu

Fair

Szekeres-Barthó

et al. 2011

Physiological Genomics

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Forde N. Endometrial expression of progesterone-induced blocking factor and galectins-1, -3, -9, and -3 binding protein in the luteal phase and early pregnancy in cattle. Physiol Genomics 43: 903-910, 2011. First published May 24, 2011 doi:10.1152/physiolgenomics.00251.2010.-Progesterone-induced blocking factor (PIBF) and galectins modulate the maternal immune response during pregnancy. We hypothesized that the relative transcript abundance of the above genes would be different during the luteal phase/early pregnancy and would be affected by progesterone supplementation. To further test this, hypothesis protein expression analyses were carried out to evaluate the abundance and localization of LGALS9 and PIBF. Following estrus synchronization, heifers were inseminated (n ϭ 140) or not (n ϭ 70). Half the heifers in each status (cyclic or potentially pregnant) were randomly assigned to receive a progesterone-releasing intravaginal device (PRID) on day 3 after estrus, which elevated progesterone concentrations from day 3.5 to 8 (P Ͻ 0.05), resulting in four treatment groups: cyclic and pregnant heifers, each with normal and high progesterone. After confirmation of pregnancy status in inseminated animals, uterine tissue was collected on days 5, 7, 13, or 16 of the luteal phase of the cycle/ pregnancy. Gene and protein expression was determined using Q-RT-PCR and IHC, respectively, on 5 heifers per treatment per time point (i.e., 80 in total). Progesterone concentrations did not affect expression of any of the genes (P Ͼ 0.05).LGALS9 and LGALS3BP were expressed at low levels in both cyclic and pregnant endometria until day 13. On day 16, expression increased only in the pregnant heifers (P Ͻ 0.0001).LGALS1 and LGALS3 decreased on day 7 (P Ͻ 0.0001) and remained low until day 16. Pregnancy had no effect on the expression of LGALS1, LGALS3, and PIBF. Additionally, LGALS9 and PIBF proteins were expressed in distinct uterine cell types. These results indicate that the galectins may be involved in uterine receptivity and/or implantation in heifers.bovine; uterus; early pregnancy; estrous cycle; progesterone DURING THE ESTROUS CYCLE, the uterus undergoes remodeling under the influence of estrogen and progesterone, to create an optimum environment for embryo survival and successful implantation. Numerous studies have identified a linear and quadratic relationship between progesterone concentrations during early pregnancy and probability of embryo survival/ pregnancy outcome in both lactating dairy cows and nonlactating heifers (12,35,52). Elevated concentrations of circulating progesterone in the immediate postconception period have been associated with an advancement of conceptus elongation (8,20,46), an increase in interferon-tau (IFNT) production (32, 33) and higher pregnancy rates in cattle and sheep (35,52

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Neonatal exposure to progesterone and estradiol alters uterine morphology and luminal protein content in adult beef heifers

Cited by 39 publications

References 28 publications

Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches

Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches

Ovine Uterine Gland Knock-Out Model: Effects of Gland Ablation on the Estrous Cycle1

Endometrial expression of progesterone-induced blocking factor and galectins-1, -3, -9, and -3 binding protein in the luteal phase and early pregnancy in cattle

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