J. Anim. Sci. 2005. 83:810-815
© 2005 American Society of Animal Science
ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Growth hormone at breeding modifies conceptus development and postnatal growth in sheep1
B. A. Costine,
E. K. Inskeep and
M. E. Wilson2
Division of Animal and Veterinary Sciences, West Virginia University, Morgantown 26506
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Abstract
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Experiments were performed to determine the effects of components of the GH-IGF axis on conceptus development and postnatal growth in sheep. In Exp. 1, ewes received one of the following treatments: 1) sustained release GH at breeding, 2) sustained release GH at breeding and estradiol-17ß at d 5 and 6, 3) only estradiol-17ß at d 5 and 6, or 4) no treatment. Uteri were flushed on d 7, and flushings were analyzed for content of IGF-I. A single injection of sustained-release bovine GH at breeding increased IGF-I content in uterine luminal flushings compared with control ewes (P < 0.05). Treatment with estradiol-17ß on d 5 and 6 after breeding did not alter IGF-I content compared with control ewes, and it blocked the effect of GH on uterine luminal IGF-I content. In Exp. 2, sustained release GH or no treatment was administered at breeding, and gravid uteri were collected at d 25, 80, or 140 of gestation. On d 80, GH-treated ewes had smaller chorioallantoic weights (P < 0.05) and tended to have more efficient placentae (fetal weight/total placental weight; P = 0.052), with a higher percentage of placental weight as cotyledons (P = 0.068) compared with control ewes. In Exp. 3, ewes were treated with or without sustained release GH at progesterone withdrawal. Lambs from GH-treated ewes were heavier at birth (P < 0.05). Lambs from GH-treated ewes reared as singles, but not lambs reared as multiples, were heavier at 30, 60 (P < 0.05), and 75 d (P = 0.075) of age than lambs from control ewes. In conclusion, ewes treated with sustained-release GH at breeding developed smaller, more efficient placentas, and had larger lambs at birth.
Key Words: Growth Factors • Growth Hormone • Placenta • Pregnancy • Sheep
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Introduction
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Growth of the placenta preceding attachment will determine the number of placentomes that will be established. From d 40 through 90, placentomes undergo proliferation, whereas the mass of the chorioallantois remains constant (Ehrhardt and Bell, 1995
). In the ewe, 80% of fetal growth occurs during the last third of gestation (Robinson et al., 1977), and growth is limited by the size and function of the placenta that developed during the first two-thirds of pregnancy (Wallace et al., 1999).
The GH system is important in embryonic development, not only for the stimulation of histotroph, but also by directly inducing alterations in gene expression and metabolism in the embryo (reviewed by Sinclair et al., 2003). In the ewe, IGF-1 mRNA is expressed in the endometrium (Stevenson et al., 1994; Cann et al., 1997b), and IGF-I in uterine flushings was greatest at estrus and d 5 and was lower by d 12 of pregnancy (Cann et al., 1998). Because luminal concentrations of IGF-I increased within 15 h of estrus (Wathes et al., 1994), Cann et al. (1998) proposed that estradiol-17ß induces IGF-I production.
Lambs with smaller birth weights have a greater mortality during the first year (Shelton, 1964; Greenwood et al., 1998), as do infants (McIntire et al., 1999). McKenzie and Bogart (1934) realized the value of placental size and "quality" as indicators of the thrift of the lamb. Twenty percent of all lambs die before weaning; 80% of deaths occur during the first few days of life (Dennis, 1972). Development is altered in low-birth-weight lambs, which is manifested by slower growth, a lower accretion of fat and nitrogen, and decreased bone development (Greenwood et al., 1998).
The hypotheses for the current experiments were suggested: 1) an injection of sustained-release GH given at breeding or treatment with estradiol-17ß on d 5 and 6 would alter luminal concentrations of IGF-1; and 2) GH given at breeding would alter conceptus development, lamb weight at birth, or postnatal growth.
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Materials and Methods
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The West Virginia University Animal Care and Use Committee approved all animal care and use procedures.
Exp. 1: Effect of Growth Hormone and Estradiol-17ß on Uterine Luminal Content of IGF-I
Mature ewes of mixed breeding were observed for estrus every 12 h with the aid of a vasectomized ram. Ewes that exhibited at least two normal estrous cycles (i.e., 15 to 18 d) were mated by a fertile ram at the onset of estrus (d 0) and again 12 h later by a different fertile ram. Ewes (n = 4 ewes per treatment) were assigned randomly to a 4 x 4 incomplete factorial arrangement of treatment groups (Table 1). Ewes received a single s.c. injection of 0, 150, 300, or 500 mg of recombinant bovine GH (Posilac; Monsanto, St. Louis Mo.) at breeding, and a s.c. injection of 0, 125, 250, or 500 µg/d of estradiol-17ß (doses shown not to cause luteolysis [Hawk and Bolt, 1970]; Sigma, St. Louis Mo.) in corn oil, on d 5 and 6. On d 7, mated ewes were anesthetized with sodium pentobarbital (Sigma; 2 mg/kg i.v.), and a mid-ventral laparotomy was performed to expose the reproductive tract. Individual uterine horns were flushed by placing a glass cannula into the tip of the uterine horn and infusing 10 mL of 10 mM phosphate-buffered (pH 7.2), 150 mM saline into the base of the horn. Uterine luminal contents were massaged toward the tip of the uterine horn and out through the glass cannula into a petri dish. Uterine flushings were pooled, centrifuged at 3,000 x g, and the supernatant was frozen at –20°C until an immunoradiometric assay (Diagnostic Laboratory Services, Honolulu, HI) was performed to determine the concentration of IGF-I in the uterine flushings, which was corrected by the volume of fluid used to flush the uterine lumen to calculate the uterine luminal IGF-I content.
The effect of dose of GH, dose of estradiol-17ß, or the combination of the two on uterine luminal IGF-I content was tested by the GLM procedure of SAS (SAS Inst., Inc., Cary, NC). Means were separated using Duncan’s multiple-range test.
Exp. 2: Effect of Growth Hormone on Fetal and Placental Development
Mature ewes of mixed breeding were bred as described in Exp. 1. Ewes were assigned randomly to receive either no treatment (n = 35) or 500 mg of recombinant bovine GH (n = 33; Posilac, the treatment that resulted in the greatest uterine luminal IGF-I content in Exp. 1) at estrus. Treated and control ewes were assigned randomly to be slaughtered, and the uteri collected on d 25 (n = 20; around the time of initial placentome development), d 80 (n = 20; just before the rapid proliferation of the cotyledonary vasculature), or on d 140 (n = 28; just before term of gestation). Each uterine horn was opened along the antimesometrial border. Number and position of conceptuses in each uterine horn were recorded. On d 25 of gestation, gravid uteri were collected, chorioallantoic fluid was drained, the fetus was separated from the placenta, and fetal weight, crown rump length, and chorioallantoic membrane weight and length were determined. In uteri collected on d 80 or 140 of gestation, fetal sex, weight, and crown rump length were recorded. Serum was collected from the jugular vein of the dam and the umbilical cord of each fetus to determine concentrations of total IGF-I. Individual cotlyedons were separated manually from caruncles. The cotyledons were removed from the chorioallantoic membrane, counted, and weighed. The remaining chorioallantoic membrane was weighed, and placental length along the lesser curvature of the placenta was measured. Maternal and fetal blood samples were centrifuged at 3,000 x g, and serum was frozen at –20° C until concentrations of total IGF-I were determined using the assay described in Exp. 1.
The effects of GH treatment, single vs. multiple fetuses per ewe, day of gestation, and the interactions on concentrations of IGF-I in maternal and fetal serum, fetal weight, crown rump length, placental length, chorioallantoic membrane weight, total placental weight, placental efficiency, cotyledonary weight, cotyledon number, and percentage of placenta composed of cotyledons were tested using the GLM procedure of SAS following log transformation of the data (placental efficiency and percentage of cotlyedons were not log transformed). In ewes that had more than one fetus, means were determined for that ewe because ewe was the experimental unit. Means were compared using the LSMEANS procedure, and correlations were performed using the CORR procedure of SAS.
Exp. 3: Effect of GH Treatment to Ewes at Breeding on Lamb Birth Weight and Growth
Estrus was synchronized in mature ewes of mixed breeding by administration of an intravaginal progesterone releasing device (InterAG, Hamilton, New Zealand) for 12 d. Ewes were assigned randomly to receive either no treatment (n = 23) or an i.m. injection of 25 mg of recombinant bovine GH (2 mL of sustained-release bovine GH; Monsanto; n = 31) at the time of progesterone withdrawal. Ewes were penned with fertile rams at a ewe:ram ratio of approximately 12:1. Estrus was determined by fitting rams with crayon marking harnesses and observing for new marks on ewes every 12 h. Jugular serum was collected from all ewes on d 6 after estrus for determination of concentrations of progesterone and IGF-I. Progesterone concentrations were determined by RIA (Sheffel et al., 1982). The intraassay CV was 11% and the sensitivity was 20 pg/mL. Concentrations of both free and total IGF-1 were determined using the assay described in Exp. 1, with and without the extraction of IGF-I from binding proteins. Pregnancy was determined, and fetuses were enumerated on d 40 of gestation by transrectal ultrasonography using an Aloka 500 console (Aloka Co. Ltd., Wallingford, CT) fitted with a 7.5-MHz transducer. At lambing, type of birth (single vs. multiple), birth weight, and sex of lamb were recorded. Lambs were raised with access to creep feed. Lambs were weighed at 30, 60, and 75 d after birth, and type of rearing (single vs. multiple) was recorded.
The effect of GH treatment on birth weight was tested using the GLM procedure of SAS. In ewes with more than one lamb, weights of lambs were averaged because ewe was the experimental unit. The effect of GH treatment, type of rearing (single vs. multiple), and the interaction on 30-, 60-, and 75-d weights were tested by repeated-measures ANOVA using the GLM procedure of SAS. The effect of GH treatment on concentrations of serum progesterone, free IGF-I, and total IGF-I on d 6 after breeding was tested using the GLM procedure of SAS, and means were separated using LSMEANS procedure.
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Results
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In Exp. 1, treatment of ewes with 500 mg of bovine GH at breeding increased (P < 0.05) uterine luminal IGF-I content compared with control ewes, whereas 150 and 300 mg of bovine GH resulted in intermediate uterine luminal IGF-I content (Figure 1). Treatment of ewes on d 5 and 6 after mating with 125, 250, or 500 µg of estradiol-17ß did not increase IGF-I content in uterine luminal flushings compared with control ewes; however, treatment with estradiol-17ß on d 5 and 6 in combination with 500 mg of bovine GH at breeding abolished the positive effect of GH on uterine luminal IGF-I content.
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Figure 1. Effect of GH, estradiol-17ß, or the combination on intraluminal content of IGF-I (n = 4 per treatment). Means ± SEM with different letters differed, P < 0.05.
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In Exp. 2, GH treatment at breeding decreased the chorioallantoic membrane weight on d 80 of gestation compared with control ewes, but GH had no effect at d 25 or 140 (Figure 2). On d 80 of gestation, placentas from ewes treated with GH tended (P = 0.068) to have a higher percentage of placental weight composed of cotyledons than placentas from control ewes (77.2 ± 2.3% vs. 57.6 ± 2.7%). In addition, placentas from treated ewes on d 80 tended (P = 0.052) to be more efficient (fetal weight/chorioallantoic weight) compared with placentas from control ewes (2.76 ± 0.20 vs. 1.28 ± 0.18). Differences in placental characteristics were no longer present at d 140 of gestation. Treatment of ewes with GH at the time of breeding did not alter fetal weight, crown rump length, placental length, cotyledonary weight, cotyledon number, or total placental weight compared with fetuses from control ewes during any stage of gestation. There was no interaction between treatment and type of gestation (single vs. multiple).
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Figure 2. Weight of the chorioallantoic membrane in conceptuses gestated in ewes treated with GH or control ewes on d 25, 80, and 140 of gestation. Means ± SEM with different letters differed, P < 0.05.
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There was no effect of GH treatment at breeding on fetal or maternal serum concentrations of total IGF-I on d 80 (fetal = 76.1 ± 3.8 ng/mL for control vs. 69.9 ± 4.4 ng/mL for treated; maternal = 487 ± 44 ng/mL for control vs. 384 ± 70 ng/mL for treated) or 140 of gestation (fetal = 157 ± 35 ng/mL for control vs. 190 ± 35 ng/mL for treated; maternal = 330 ± 76 ng/mL for control vs. 332 ± 51 ng/ mL for treated). Mean serum concentrations of IGF-I were higher in fetuses gestated as singles compared with fetuses gestated as multiples at d 140 (266.1 ± 40.7 vs. 97.7 ± 8.9 ng/mL; P < 0.05), but not at d 80 (78.2 ± 3.3 vs. 69.5 ± 4.2 ng/mL). Fetal weight (r = 0.59; P < 0.0001), chorioallantoic weight (r = 0.41; P < 0.05), cotyledon number (r = 0.37; P < 0.05), and total placental efficiency (fetal weight/total placental weight; r = 0.29; P < 0.05) were positively correlated with fetal concentrations of IGF-I. Concentrations of IGF-I in maternal serum tended to decrease between d 80 and term (435 ± 42 vs. 331 ± 44 ng/mL; P = 0.10). Concentrations of IGF-I in fetal serum doubled between d 80 of gestation and term (73.0 ± 2.9 vs. 172.6 ± 24.6; P < 0.05).
In Exp. 3, concentrations of both free and total IGF-I in jugular serum on d 6 after breeding were higher (P < 0.05) in ewes treated with GH than in ewes that received no treatment (4.37 ± 0.68 vs. 0.70 ± 0.04 ng/mL of free IGF-I; 489.6 ± 5.4 vs. 177.3 ± 13.3 ng/mL of total IGF-I). There was no difference in jugular serum concentrations of progesterone between GH-treated and control ewes on d 6 after breeding (2.8 ± 0.2 vs. 2.4 ± 0.2 ng/ mL, respectively). There was a main effect of GH on lamb weight at birth (5.06 ± 0.20 for treated vs. 4.55 ± 0.15 kg for control; P < 0.05). At d 30, 60 (P < 0.05), and 75 (P = 0.075), GH treatment at breeding resulted in heavier BW of lambs reared as singles, but not of lambs reared as multiples (Figure 3).
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Figure 3. Weights of lambs reared as singles or multiples gestated in ewes treated with GH or control ewes at d 30 (A), 60 (B), and 75 (C). Means ± SEM with different letters differed within day (a, b; P < 0.05). Means ± SEM with different letters tended to differ within day (c, d; P = 0.075).
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Discussion
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A single injection of GH at breeding increased uterine luminal concentrations of IGF-1 and altered placental and fetal development. Similar dramatic effects of hormones early in gestation have previously been demonstrated in the sow. Treatment of Meishan sows with estradiol-17ß during the time of embryonic elongation at d 12 and 13 increased intraluminal concentrations of IGF-I and resulted in larger and less efficient placentas (Wilson and Ford, 2000). In the present experiment, treatment with estradiol-17ß eliminated the GH-stimulated increase in IGF-I content in the uterine lumen, in contrast with the sow, in which the increased secretion of estradiol-17ß by the embryo was accompanied by increased uterine luminal IGF-I (Simmen et al., 1990; Green et al., 1995; Wilson and Ford, 1997). Previous experiments in ewes have demonstrated a stimulatory effect of estradiol-17ß on uterine luminal IGF-I content, but in those experiments, the estradiol-17ß was unopposed by progesterone (Wathes et al., 1998; Cann et al., 1997a). In the current experiment, ewes were treated with estradiol-17ß during the luteal phase.
Growth hormone or the GH-stimulated production of IGF-I by the liver and by the endometrium (Pershing et al., 2002) may have altered conceptus development directly or indirectly via the endometrial glands. Serum concentrations of GH may have been elevated for at least 15 d (Cushman et al., 2001). Endometrial glands express receptors for GH as early as d 8 of pregnancy (Lacroix et al., 1999), and mRNA for IGF type 1 receptor is greatest on d 13 to 18 during pregnancy (Reynolds et al., 1997). Histotroph production by endometrial glands is initiated before d 14 of gestation (Ing et al., 1989), and histotroph production may have been increased in GH-treated ewes directly by GH or indirectly by IGF-I. Infusion of GH into the uterine lumen increased the density and diameter of endometrial glands (Noel et al., 2003), and upregulated uterine milk protein mRNA expression in ovariectomized ewes treated with progesterone (Spencer et al., 1999). This effect seems to be a direct effect of GH, as GH infusion did not increase either IGF-I or IGF-II compared with control ewes (Noel et al., 2003). Growth hormone or IGF-1 may have directly altered conceptus development. Pig embryos have receptors for IGF-1, and trophectoderm mitotic rate is stimulated by IGF-1 treatment (Lewis et al., 1992). Treatment of embryos in vitro with GH stimulated mitosis of the trophectoderm (Markham and Kaye, 2003); however, in the present experiment, the membrane that develops from the trophectoderm was actually smaller in GH-treated ewes, indicating that GH, or GH-stimulated IGF-I, is most likely acting indirectly via the endometrial glands.
In Exp. 2, GH treatment resulted in placentas with decreased chorioallantoic weights compared with controls, which developed in a manner more like the normal pattern for ovine placental growth characterized by Ehrhardt and Bell (1995). A smaller and more efficient chorioallantois at d 80 may have resulted from greater absorption of histotroph, particularly very early in gestation. During the first two trimesters, when organogenesis occurs, the fetus mainly depends on the absorption of histotrophic nutrition by the chorioallantois (Roberts and Bazer, 1988). Vascularization of the placentomes and the accompanying exponential increase in uterine blood flow do not occur until after d 100 of gestation (Reynolds and Redmer, 1995). In the last trimester, when 70% of the increase in fetal weight occurs, fetal nutrition is primarily hematotrophic (Green, 1946). Although there was no effect of GH on placentomal weight or number, cotyledons comprised a greater percentage of placental weight in placentas of fetuses gestated in ewes treated with GH, indicating that the placenta may have had a similar number of attachments to the maternal endometrium, but in a smaller surface area. Variations in placentomal vascularity can occur without alterations in gross measurements (Vonnahme et al., 2003). Further experiments are needed to determine whether GH treatment affects placentomal vascularity.
Treatment of ewes at breeding with sustained-release GH resulted in heavier lambs at birth, and this weight increase continued through postnatal development in lambs reared as singles. It is known that fetal development affects both birth weight and postnatal development. Nutrient restriction, utilized to alter placental and fetal growth, concomitantly activate the maternal hypo-thalamic-pituitary-adrenal axis (Wallace et al., 1997, 1999; Lesage et al., 2001). Nutrient restriction of ewes during mid-gestation altered fetal and placental development, similar to an infusion of cortisol on d 119 to 129, which altered placental growth, resulting in smaller fetuses with increased cardiac ventricular wall thickness (Vonnahme et al., 2003; Jensen et al., 2002). In the current experiments, placental development was altered in the likely absence of general activation of the maternal hypothalamic-pituitary-adrenal axis, and therefore, GH treatment of ewes at breeding may provide a useful model to study placental development.
The increase in birth weight in response to GH observed in Exp. 3 might be due to an increase in placental efficiency similar to that observed in Exp. 2. There was a main effect of GH treatment on chorioallantoic weight at d 80, despite large variations in chorioallantoic weight in single vs. multiple conceptuses. Placental efficiency has mainly been examined in the pig. Increased placental efficiency is hypothesized to be the mechanism by which the Meishan pig has three to five more pigs per litter than U.S. pig breeds (Wilson et al., 1999; Wilson and Ford, 2000, 2001). The magnitude of change in placental efficiency between conceptuses from GH-treated ewes (2.7) and controls (1.2) is similar to the magnitude of difference in placental efficiency between the Meishan pig (8.7) and the Yorkshire (3.4; [Ford, 1997]). The importance of placental efficiency rather than placental size is further emphasized by the positive correlation of post-natal survival with placental efficiency and the negative correlation of postnatal survival with placental size (Leenhouwers et al., 2002).
Maintenance of the effect of GH on weight in lambs reared as singles may have been due to greater milk availability in the absence of competition from a littermate. In addition, the amount of lactogen synthesized by the placenta is positively correlated with placental size (Wallace et al., 1997, 2003). In the current experiment, placentas were larger in ewes gestating a single lamb, potentially increasing the degree of mammogenesis and lactogenesis during pregnancy. Nonetheless, the increased weight of single lambs from GH-treated ewes continued beyond weaning, which may be due to altered GH-IGF-1 axis, which was only manifested in single lambs. The effect of GH at breeding on placental production of lactogen and the effect on the postnatal GH-IGF-1 axis require further study.
In conclusion, administration of sustained-release GH at breeding resulted in increased intraluminal content of IGF-I for at least 7 d, and altered conceptus development such that placentas were smaller and more efficient compared with conceptuses gestated in control ewes. Lambs born from ewes treated with GH were heavier at birth, and single lambs maintained the increase in BW through 75 d of age.
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Implications
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A greater understanding of how alterations in the uterine environment very early in gestation influence the growth and development of offspring should ultimately translate into improvements in nutrition and management that promote optimal growth and development of the individual prenatally, such that postnatal growth and production may be optimized.
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Footnotes
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1 This work is published with the approval of the Director of WV Agric. and Forage Exp. Stn. as Scientific Paper No. 2886. This project was supported by National Research Initiative Competitive Grant No. 2001-35203-10982 to M. E. Wilson from the USDA Cooperative State Research, Education, and Extension Service and Hatch Project 321 (NE 161). 
2 Correspondence: G048 Agric. Sci. Bldg. (phone: 304-293-2631, ext. 4425; fax: 304-293-2232; e-mail: mwilso25{at}wvu.edu).
Received for publication September 27, 2004.
Accepted for publication December 18, 2004.
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G. Wu, F. W. Bazer, J. M. Wallace, and T. E. Spencer
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J Anim Sci,
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Abstract
Introduction
