Polyamine Synthesis from Proline in the Developing Porcine Placenta1

Abstract

Polyamines (putrescine, spermidine, and spermine) are essential for placental growth and angiogenesis. However, little is known about polyamine synthesis in the porcine placenta during conceptus development. The present study was conducted to test the hypothesis that arginine and proline are the major sources of ornithine for placental polyamine production in pigs. Placentae, amniotic fluid, and allantoic fluid were obtained from gilts on Days 20, 30, 35, 40, 45, 50, 60, 90, and 110 of the 114-day gestation (n = 6 per day). Placentae as well as amniotic and allantoic fluids were analyzed for arginase, proline oxidase, ornithine aminotransferase (OAT), ornithine decarboxylase (ODC), proline transport, concentrations of amino acids and polyamines, and polyamine synthesis using established radiochemical and chromatographic methods. Neither arginase activity nor conversion of arginine into polyamines was detected in the porcine placenta. In contrast, both proline and ornithine were converted into putrescine, spermidine, and spermine in placental tissue throughout pregnancy. The activities of proline oxidase, OAT, and ODC as well as proline transport, polyamine synthesis from proline, and polyamine concentrations increased markedly between Days 20 and 40 of gestation, declined between Days 40 and 90 of gestation, and remained at the reduced level through Day 110 of gestation. Proline oxidase and OAT, but not arginase, were present in allantoic and amniotic fluids for the production of ornithine (the immediate substrate for polyamine synthesis). The activities of these two enzymes as well as the concentrations of ornithine and total polyamines in fetal fluids were highest at Day 40 but lowest at Days 20, 90, and 110 of gestation. These results indicate that proline is the major amino acid for polyamine synthesis in the porcine placenta and that the activity of this synthetic pathway is maximal during early pregnancy, when placental growth is most rapid. Our novel findings provide a new base of information for future studies to define the role of proline in fetoplacental growth and development.

Effects of dietary arginine supplementation on reproductive performance and immunity of sows

“…The reduction in dead pigs in Arg-supplemented sows may be ascribed to the improved uterine capacity (Wu et al, 2006;Mateo et al, 2007). Arg is required for placental synthesis of both NO and polyamines, which do not only stimulate placental angiogenesis and vascular growth, but also utero-placental blood flow and maternal nutrients transfer (Wu et al, 2005), thereby developing an efficient uterine capacity for fetal growth and development (Reynolds et al, 2001;Kwon et al, 2004;Wu et al, 2006). Both NO and polyamines have been considered as one of the major factors contributing to intrauterine growth restriction (Wu et al, , 2006.…”

Comparative aspects of implantation

“…ODC1 can regulate conceptus development and differentiation by catalyzing the synthesis of polyamines that associate with DNA and nuclear proteins to produce normal chromatin required for proliferation of trophectoderm and formation of multinucleated trophectoderm cells (see Bachrach et al 2001). ODC1 and polyamines are important for trophectoderm motility and receptivity of uterine epithelial cells to adhesion by trophectoderm of mouse blastocysts (Martin et al 2003), rapid growth of the placenta and fetus, as well as increases in placental blood flow in pigs and sheep (see Wu et al 2005). NO promotes blastocyst attachment and trophectoderm motility, possibly through modifications of the ECM, and stimulation of vasodilation of maternal capillaries, through PI3K/AKT/FRAP1 induced by HGF, and/or by stimulating expression of SPP1 (see Guo et al 2005).…”

Pregnancy recognition signals in mammals: the roles of interferons and estrogens

“…These observations indicate different strategies for arginine metabolism among gestating mammals and suggested important biological roles for Arg in growth and development of mammalian conceptuses. Accordingly, rates of NO and polyamine synthesis in both porcine and ovine placentae are highest during early gestation when placental growth is most rapid (Kwon et al, 2004a, b;Wu et al, 2005Wu et al, , 2012. We hypothesize that impaired placental growth (including vascular growth) or function results from reduced placental synthesis of NO and polyamines, thereby contributing to IUGR in both underfed and overfed dams .…”