Abstract
The placenta is a highly efficient multifunctional organ, mediating the exchange of nutrients, gases and waste products between the dam and fetus. This study investigated the effects of chronic maternal undernutrition (70% of estimated requirement) on the placental growth trajectory in the ewe on days 45, 90 and 135 of gestation. The insulin-like growth factor (IGF) system was investigated using in situ hybridisation analysis to determine if nutritionally mediated alterations in placental growth were regulated through modifications in placental IGF expression. Placental weight increased between days 45 and 90 (P<0.01), accompanied by a reduction in maternal placentome IGF binding protein (IGFBP)-3, -5 and -6 expression (P<0.05), although IGF-II mRNA levels in maternal villi remained unchanged. Placentome number was unaffected by diet or gestational age. Placental weight remained constant between days 90 and 135 in ewes on 100% maintenance rations but decreased over this period (P<0.05) in ewes on the 70% rations. Gross morphology also altered, so the underfed ewes had more type C and type D placentomes and fewer type B placentomes than their well-fed counterparts on day 135 (P<0.05). These changes were accompanied by higher IGFBP-6 mRNA expression in the maternal placental villi in undernourished ewes (P<0.05). The change in shape from a type A to a type C placentome was accompanied by flattening of the placentome and a reduction in the ratio of the area of unattached fetal allantochorion to interdigitated maternal and fetal villi. Within the intercotyledonary endometrium, expression of IGFBPs-3 and -5 mRNA in the glandular epithelium increased between days 45 and 90, showing an opposite trend with time to that found in the adjacent placentomes. This indicates tissue-specific control of IGFBP expression. In conclusion, this study has shown clear time-related changes in the uterine IGFBP system during pregnancy, which accompany changes in placental growth. Altered IGFBP expression may play a role in determining placental size in relation to nutritional status, but is unlikely to be the only mediator.
Highlights
The placenta is an important determinant of fetal growth, with placental size and birthweight being positively correlated in many species, including sheep (Mellor 1983, Kelly 1992)
The placentomes reach a maximum weight by approximately day 75 to 80 of gestation whilst 80% of fetal growth occurs in the final third of gestation (Ehrhardt & Bell 1995, Wallace et al 1999)
Evidence suggests that the insulin-like growth factor (IGF) system, a nutritionally sensitive group of proteins, has a fundamental role in placental and fetal development (Reynolds et al 1997, Wathes et al 1998, Han & Carter 2000)
Summary
The placenta is an important determinant of fetal growth, with placental size and birthweight being positively correlated in many species, including sheep (Mellor 1983, Kelly 1992). Evidence suggests that the insulin-like growth factor (IGF) system, a nutritionally sensitive group of proteins, has a fundamental role in placental and fetal development (Reynolds et al 1997, Wathes et al 1998, Han & Carter 2000). These findings are supported by gene deletion studies in mice (Baker et al 1993, Liu et al 1993). A family of high affinity insulin-like growth factor binding proteins (IGFBPs), designated IGFBP-1 to -6, regulate the biological activities of the IGFs (Rechler & Clemmons 1998, Journal of Endocrinology (2004) 182, 89–103 0022–0795/04/0182–089 2004 Society for Endocrinology Printed in Great Britain
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