Maternal endocrine adaptation throughout pregnancy to nutrient manipulation: Consequences for sexually dimorphic programming of thyroid hormones and development of their progeny

Abstract

Maternal nutrient restriction during critical windows of fetal development alters postnatal growth, often in a sexually dimorphic manner. Intrauterine growth restriction is frequently characterized by accelerated growth and increased adiposity in later life. Thyroid hormones are implicated as part of the mechanism involved in this scenario via their actions within the hypothalamic-pituitary-thyroid axis. We fed high (H = 240%) and low (L = 70%) levels of recommended daily crude protein intake during the first and second trimesters of gestation to beef heifers to investigate effects to their progeny's plasma concentrations of free and total triiodothyronine (FT3 and TT3) and thyroxine (FT4 and TT4) from birth until weaning at 191 days of age (n = 68). The study design was a two-by-two factorial. For male progeny, exposure to maternal diets low in protein during the first trimester of gestation resulted in greater FT4 at birth (P < 0.05) which was subsequent to lower concentrations of leptin in maternal plasma at 271 days of gestation compared with their high-protein-exposed counterparts. These same animals went on to have greater milk intake during the latter half of the lactation period (P < 0.05) and exhibited faster rates of average daily gain (ADG) relative to birth weight during this time (P < 0.05). For all progeny, independent of sex, exposure to low-protein maternal diets during the second trimester of gestation resulted in greater FT3 relative to TT3 at birth. Because FT3 at birth and 29 days was positively associated with ADG (P < 0.05) and ADG relative to birth weight (P < 0.05), it is proposed that FT3 plays an integral role in catch-up growth in the bovine as per other species. Protein intake during the first and second trimesters of gestation has a sexually dimorphic effect on progeny plasma thyroid hormone concentrations, and these changes are associated with altered milk intake and postnatal growth pathway.

Fetal programming in 2-year-old calving heifers: peri-conception and first trimester protein restriction alters fetal growth in a gender-specific manner

“…The sexual dimorphism observed, such that the effect peri-conception protein restriction effect was greater in the male, supports our previous findings in beef cattle (Micke et al 2011(Micke et al , 2014. This suggests that the male embryo is more susceptible to early gestational intervention than the female, as seen in the in vitro embryo (Bermejo-Alvarez et al 2011), and that this effect continues until at least 98dpc.…”

Peri-conception and first trimester diet modifies reproductive development in bulls

“…This in utero effect was, however, not discernible in later gross measures such as birthweight or postnatal growth as previously reported in lambs (Kotsampasi et al 2009) or calves (Micke et al 2015) but effects upon postnatal reproductive development were evident: the LPeri diet decreased blood vessel area in the fetal testis. Moreover, seminiferous tubule number and percentage was increased, although this effect was not evident in the adult.…”

Epigenetics and developmental programming of welfare and production traits in farm animals

“…Micke et al (2015) reported that protein intake in the first and second trimesters has sexually dimorphic effects on progeny appetite and postnatal growth pathways and that this is associated with altered circulating thyroid hormone and leptin concentrations in the progeny. In contrast, no differences in food intake (at 26-30 months of age) were attributed to wide differences in prenatal growth and birthweight (Greenwood and Cafe 2007).…”

“…In general, reducing calf birthweight by means of maternal dietary restriction does not reduce the incidence of dystocia or calf morbidity. This is due to both effects on maternal physiology (Micke et al 2015) and changes to the immune status of the calf and colostrum (McGee et al 2006). However, in a few studies cow nutrition has been linked to calf mortality (e.g.…”