Maternal citrulline supplementation enhances placental function and fetal growth in a rat model of IUGR: involvement of insulin-like growth factor 2 and angiogenic factors

References

• Katz J, Lee AC, Kozuki N, et al. Mortality risk in preterm and small-for-gestational-age infants in low-income and middle-income countries: a pooled country analysis. Lancet 2013;382:417–25
   PubMed Web of Science ®Google Scholar
• Barker DJ. Adult consequences of fetal growth restriction. Clin Obstet Gynecol 2006;49:270–83
   PubMed Web of Science ®Google Scholar
• Sibley CP, Brownbill P, Dilworth M, Glazier JD. Review: adaptation in placental nutrient supply to meet fetal growth demand: implications for programming. Placenta 2010;31:S70–4
   PubMed Web of Science ®Google Scholar
• Dorniak-Wall T, Grivell RM, Dekker GA, et al. The role of L-arginine in the prevention and treatment of pre-eclampsia: a systematic review of randomised trials. J Human Hypertens 2014;28:230–5
   PubMed Web of Science ®Google Scholar
• Winer N, Branger B, Azria E, et al. L-Arginine treatment for severe vascular fetal intrauterine growth restriction: a randomized double-bind controlled trial. Clin Nutr 2009;28:243–8
   PubMed Web of Science ®Google Scholar
• Krause BJ, Carrasco-Wong I, Caniuguir A, et al. Endothelial eNOS/arginase imbalance contributes to vascular dysfunction in IUGR umbilical and placental vessels. Placenta 2013;34:20–8
   PubMed Web of Science ®Google Scholar
• Laskowska M, Laskowska K, Leszczynska-Gorzelak B, Oleszczuk J. Asymmetric dimethylarginine in normotensive pregnant women with isolated fetal intrauterine growth restriction: a comparison with preeclamptic women with and without intrauterine growth restriction. J Matern Fetal Neonatal Med 2011;24:936–42
   PubMed Web of Science ®Google Scholar
• Curis E, Nicolis I, Moinard C, et al. Almost all about citrulline in mammals. Amino Acids 2005;29:177–205
   PubMed Web of Science ®Google Scholar
• Bourdon A, Parnet P, Nowak C, et al. l-Citrulline supplementation enhances fetal growth and protein synthesis in rats with intrauterine growth restriction. J Nutr 2016;146:532–41
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402–8
   PubMed Web of Science ®Google Scholar
• Furukawa S, Hayashi S, Usuda K, et al. Toxicological pathology in the rat placenta. J Toxicol Pathol 2011;24:95–111
   PubMed Web of Science ®Google Scholar
• Fowden AL, Sferruzzi-Perri AN, Coan PM, et al. Placental efficiency and adaptation: endocrine regulation. J Physiol (Lond) 2009;587:3459–72
   Google Scholar
• Georgiades P, Ferguson-Smith AC, Burton GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 2002;23:3–19
   PubMed Web of Science ®Google Scholar
• Sferruzzi-Perri AN, Vaughan OR, Coan PM, et al. Placental-specific Igf2 deficiency alters developmental adaptations to undernutrition in mice. Endocrinology 2011;152:3202–12
   PubMed Web of Science ®Google Scholar
• Constancia M, Angiolini E, Sandovici I, et al. Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc Natl Acad Sci USA 2005;102:19219–24
   PubMed Web of Science ®Google Scholar
• Coan PM, Fowden AL, Constancia M, et al. Disproportional effects of Igf2 knockout on placental morphology and diffusional exchange characteristics in the mouse. J Physiol (Lond) 2008;586:5023–32
   Google Scholar
• Dikalova A, Fagiana A, Aschner JL, et al. Sodium-coupled neutral amino acid transporter 1 (SNAT1) modulates L-citrulline transport and nitric oxide (NO) signaling in piglet pulmonary arterial endothelial cells. PLoS One 2014;9:e85730
   PubMed Web of Science ®Google Scholar
• Connelly L, Jacobs AT, Palacios-Callender M, et al. Macrophage endothelial nitric-oxide synthase autoregulates cellular activation and pro-inflammatory protein expression. J Biol Chem 2003;278:26480–7
   PubMed Web of Science ®Google Scholar
• Demir R, Kayisli UA, Seval Y, et al. Sequential expression of VEGF and its receptors in human placental villi during very early pregnancy: differences between placental vasculogenesis and angiogenesis. Placenta 2004;25:560–72
   PubMed Web of Science ®Google Scholar
• Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995;376:66–70
   PubMed Web of Science ®Google Scholar
• Ahmad S, Hewett PW, Al-Ani B, et al. Autocrine activity of soluble Flt-1 controls endothelial cell function and angiogenesis. Vasc Cell 2011;3:15
   PubMedGoogle Scholar
• Tal R, Shaish A, Barshack I, et al. Effects of hypoxia-inducible factor-1alpha overexpression in pregnant mice: possible implications for preeclampsia and intrauterine growth restriction. Am J Pathol 2010;177:2950–62
   PubMed Web of Science ®Google Scholar
• Herr F, Liang OD, Herrero J, et al. Possible angiogenic roles of insulin-like growth factor II and its receptors in uterine vascular adaptation to pregnancy. J Clin Endocrinol Metab 2003;88:4811–17
   PubMed Web of Science ®Google Scholar
• Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem 1998;273:13313–16
   PubMed Web of Science ®Google Scholar
• Itoh S, Brawley L, Wheeler T, et al. Vasodilation to vascular endothelial growth factor in the uterine artery of the pregnant rat is blunted by low dietary protein intake. Pediatr Res 2002;51:485–91
   PubMed Web of Science ®Google Scholar
• Rutland CS, Latunde-Dada AO, Thorpe A, et al. Effect of gestational nutrition on vascular integrity in the murine placenta. Placenta 2007;28:734–42
   PubMed Web of Science ®Google Scholar
• Jansson N. Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet. J Physiol (Lond) 2006;576:935–46
   Google Scholar
• Glazier JD, Cetin I, Perugino G, et al. Association between the activity of the system A amino acid transporter in the microvillous plasma membrane of the human placenta and severity of fetal compromise in intrauterine growth restriction. Pediatr Res 1997;42:514–19
   PubMed Web of Science ®Google Scholar
• Powers R, Weissgerber TL, McGonigal S, et al. [7-or]: L-Citrulline administration increases the arginine/ADMA ratio, decreases blood pressure and improves vascular function in obese pregnant women. Pregn Hypertens 2015;5:4
   Google Scholar