Maternal exercise and growth restriction in rats alters placental angiogenic factors and blood space area in a sex-specific manner

Yeukai Tm Mangwiro; Jessica F Briffa; Sogand Gravina; Dayana Mahizir; Kristina Anevska; Tania Romano; Karen M Moritz; James Sm Cuffe; Mary E Wlodek

doi:10.1016/j.placenta.2018.12.005

Maternal exercise and growth restriction in rats alters placental angiogenic factors and blood space area in a sex-specific manner

Placenta. 2018 Dec 15:74:47-54. doi: 10.1016/j.placenta.2018.12.005. Epub 2018 Dec 15.

Authors

Yeukai Tm Mangwiro¹, Jessica F Briffa², Sogand Gravina², Dayana Mahizir², Kristina Anevska³, Tania Romano³, Karen M Moritz⁴, James Sm Cuffe⁵, Mary E Wlodek⁶

Affiliations

¹ Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC, 3083, Australia; Department of Physiology, The University of Melbourne, Parkville, VIC, 3010, Australia.
² Department of Physiology, The University of Melbourne, Parkville, VIC, 3010, Australia.
³ Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC, 3083, Australia.
⁴ School of Biomedical Sciences, The University of Queensland, St. Lucia, QLD, 4072, Australia; Child Health Research Centre, The University of Queensland, South Brisbane, Queensland, 4101, Australia.
⁵ School of Biomedical Sciences, The University of Queensland, St. Lucia, QLD, 4072, Australia.
⁶ Department of Physiology, The University of Melbourne, Parkville, VIC, 3010, Australia. Electronic address: m.wlodek@unimelb.edu.au.

PMID: 30638632
DOI: 10.1016/j.placenta.2018.12.005

Abstract

Fetal growth and development are dependent on adequate placental nutrient transfer. The surface area of the placental villous network is a key determinant of nutrient exchange, which is regulated by vasculogenic and angiogenic factors. These factors are altered by intrauterine growth restriction (IUGR) and maternal obesity in both the first (F1) and second (F2) generations. We investigated the impact of endurance exercise in IUGR dams fed a High-fat diet on placental vasculogenesis and angiogenesis. Uteroplacental insufficiency (Restricted) or sham (Control) surgery was induced on embryonic day (E) 18 in Wistar-Kyoto rats. F1 offspring were fed a Chow or High-fat diet from weaning, and at 16 weeks were further allocated an exercise protocol; Sedentary, Exercised prior to and during pregnancy (Exercise), or Exercised during pregnancy only (PregEx). Females were mated (20 weeks) and F2 placentae collected at E20. Maternal Restriction, High-fat feeding and Exercise had a minimal impact on placental regulators of vasculogenesis and angiogenesis. However, Restriction increased placental labyrinth tissue area in Chow-fed dams. PregEx induced overt adaptations, including increased VEGFA and decreased PLGF protein expression, and reduced blood space area. These alterations were sex-dependent and associated with alterations in miRNA27a, a known regulator of VEGF translation. These data highlight that maternal exercise initiated during pregnancy (PregEx) causes alterations in placental vasculogenesis and angiogenesis in a sex-dependent manner, with minimal Restriction and maternal diet effects. However, further investigation is required to determine if these adaptations are beneficial or harmful for maternal and fetoplacental outcomes.

Keywords: Angiogenesis; Exercise; Fetal programming; Growth restriction; Placenta; Vasculogenesis.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Diet, High-Fat
Female
Fetal Growth Retardation / pathology
Fetal Growth Retardation / physiopathology*
Male
Neovascularization, Physiologic
Physical Conditioning, Animal / physiology*
Placenta / blood supply
Placenta / metabolism*
Placenta / pathology
Placenta Growth Factor / metabolism
Placentation*
Pregnancy
Prenatal Exposure Delayed Effects*
Rats, Inbred WKY
Vascular Endothelial Growth Factor A / metabolism

Substances

Pgf protein, rat
Vascular Endothelial Growth Factor A
vascular endothelial growth factor A, rat
Placenta Growth Factor