Maternal dietary manganese protects chick embryos against maternal heat stress via epigenetic-activated antioxidant and anti-apoptotic abilities

Yongwen Zhu; Lin Lu; Xiudong Liao; Wenxiang Li; Liyang Zhang; Cheng Ji; Xi Lin; Hsiao-Ching Liu; Jack Odle; Xugang Luo

doi:10.18632/oncotarget.20804

Maternal dietary manganese protects chick embryos against maternal heat stress via epigenetic-activated antioxidant and anti-apoptotic abilities

Oncotarget. 2017 Sep 11;8(52):89665-89680. doi: 10.18632/oncotarget.20804. eCollection 2017 Oct 27.

Authors

Yongwen Zhu^#^{1

2

3}, Lin Lu^#¹, Xiudong Liao¹, Wenxiang Li³, Liyang Zhang¹, Cheng Ji³, Xi Lin⁴, Hsiao-Ching Liu⁴, Jack Odle⁴, Xugang Luo¹

Affiliations

¹ Mineral Nutrition Research Division, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China.
² College of Animal Science, South China Agricultural University, Guangzhou 510000, China.
³ College of Animal Science and Technology, China Agricultural University, Beijing 100193, China.
⁴ Department of Animal Science, North Carolina State University, Raleigh, NC 27695, USA.

^# Contributed equally.

Abstract

Maternal heat stress induced the aberrant epigenetic patterns resulting in the abnormal development of offspring embryos. It is unclear whether maternal dietary manganese supplementation as an epigenetic modifier could protect the chick embryonic development against maternal heat stress via epigenetic mechanisms. To test this hypothesis using an avian model, a completely randomized design with a 2 (maternal normal and high environmental temperatures of 21 and 32°C, respectively) × 3 (maternal dietary manganese sources, the control diet without manganese supplementation and the control diet + 120 mg/kg as either inorganic or organic manganese) factorial arrangement was adopted. Maternal environmental hyperthermia increased mRNA expressions of heat shock proteins 90 and 70, cyclin-dependent kinase 6 and B-cell CLL/lymphoma 2-associated X protein displaying oxidative damage and apoptosis in the embryonic heart. Maternal environmental hyperthermia impaired the embryonic development associated with the alteration of epigenetic status, as evidenced by global DNA hypomethylation and histone 3 lysine 9 hypoacetylation in the embryonic heart. Maternal dietary manganese supplementation increased the heart anti-apoptotic gene B-cell CLL/lymphoma 2 expressions under maternal environmental hyperthermia and manganese superoxide dismutase enzyme activity in the embryonic heart. Maternal dietary organic Mn supplementation effectively eliminated the impairment of maternal environmental hyperthermia on the embryonic development. Maternal dietary manganese supplementation up-regulated manganese superoxide dismutase mRNA expression by reducing DNA methylation and increasing histone 3 lysine 9 acetylation of its promoter. It is suggested that maternal dietary manganese addition could protect the chick embryonic development against maternal heat stress via enhancing epigenetic-activated antioxidant and anti-apoptotic abilities.

Keywords: apoptosis; chick embryo; epigenetics; manganese superoxide dismutase; maternal environmental hyperthermia.