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. 2019 Nov 19:10:87.
doi: 10.1186/s40104-019-0396-8. eCollection 2019.

Maternal betaine suppresses adrenal expression of cholesterol trafficking genes and decreases plasma corticosterone concentration in offspring pullets

Halima Abobaker  1   2 , Yun Hu  1   2 , Nagmeldin A Omer  1   2   3 , Zhen Hou  1   2 , Abdulrahman A Idriss  1   2 , Ruqian Zhao  1   2
Affiliations

Maternal betaine suppresses adrenal expression of cholesterol trafficking genes and decreases plasma corticosterone concentration in offspring pullets

Halima Abobaker et al. J Anim Sci Biotechnol. .

Abstract

Background: Laying hens supplemented with betaine demonstrate activated adrenal steroidogenesis and deposit higher corticosterone (CORT) in the egg yolk. Here we further investigate the effect of maternal betaine on the plasma CORT concentration and adrenal expression of steroidogenic genes in offspring pullets.

Results: Maternal betaine significantly reduced (P < 0.05) plasma CORT concentration and the adrenal expression of vimentin that is involved in trafficking cholesterol to the mitochondria for utilization in offspring pullets. Concurrently, voltage-dependent anion channel 1 and steroidogenic acute regulatory protein, the two mitochondrial proteins involved in cholesterol influx, were both down-regulated at mRNA and protein levels. However, enzymes responsible for steroid syntheses, such as cytochrome P450 family 11 subfamily A member 1 and cytochrome P450 family 21 subfamily A member 2, were significantly (P < 0.05) up-regulated at mRNA or protein levels in the adrenal gland of pullets derived from betaine-supplemented hens. Furthermore, expression of transcription factors, such as steroidogenic factor-1, sterol regulatory element-binding protein 1 and cAMP response element-binding protein, was significantly (P < 0.05) enhanced, together with their downstream target genes, such as 3-hydroxy-3-methyl-glutaryl-coenzyme A reductase, LDL receptor and sterol regulatory element-binding protein cleavage-activating protein. The promoter regions of most steroidogenic genes were significantly (P < 0.05) hypomethylated, although methyl transfer enzymes, such as AHCYL, GNMT1 and BHMT were up-regulated.

Conclusions: These results indicate that the reduced plasma CORT in betaine-supplemented offspring pullets is linked to suppressed cholesterol trafficking into the mitochondria, despite the activation of cholesterol and corticosteroid synthetic genes associated with promoter hypomethylation.

Keywords: Adrenal gland; Chicken; Cholesterol; Corticosterone; Maternal betaine; Steroidogenesis.

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Conflict of interest statement

Competing interestsThe authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Plasma corticosterone, total cholesterol and adrenal expression of cholesterol trafficking genes in pullets. a) Plasma total cholesterol; b) Plasma corticosterone c) mRNA abundance of genes involved in cholesterol trafficking d) StAR protein expression. Values are means ± SEM, *P < 0.05, compared with control for the mRNA (n = 7), for protein expression (n = 4)
Fig. 2
Fig. 2
Adrenal expression of cholesterol metabolic genes in pullets. a) Cholesterol biosynthetic genes mRNA expression; b) SREBP1 protein expression; c) HMGCR protein expression. Values are means ± SEM, *P < 0.05, compared with control for the mRNA (n = 7), for protein expression (n = 4)
Fig. 3
Fig. 3
Adrenal expression of transcription factors and downstream corticosteroid biosynthetic enzymes in pullets. a) SF-1 and CREB mRNA expression b) CREB protein expression; c) mRNA expression of corticosteroid biosynthesis enzymes; d) CYP11A1 protein expression. Values are means ± SEM, *P < 0.05, compared with control for the mRNA (n = 7), for protein expression (n = 4)
Fig. 4
Fig. 4
Adrenal expression of methionine metabolic genes in pullets. a) Schematic diagram of methionine cycle; b) Adrenal expression of key enzymes involved in methionine metabolic cycle at the mRNA; c) AHCYL protein expression; d) BHMT protein expression; e) GNMT1 protein expression; f) DNMT1 protein expression. Values are means ± SEM, *P < 0.05, compared with control. mRNA (n = 7), for protein expression (n = 4)
Fig. 5
Fig. 5
DNA methylation of cholesterol trafficking gene promoters in adrenal glands of pullets. a) Schematic diagram showing the amplified segments (S) on the promoter sequence of VIM. b) DNA methylation status on the promoter of VIM; c) Schematic diagram showing the amplified StAR segments (S); d) DNA methylation status on the promoter of StAR; e) Schematic diagram showing the amplified VDAC1 (S); f) DNA methylation status on the promoter of VDAC1. Values are means ± SEM, *P < 0.05, compared with control (n = 3)
Fig. 6
Fig. 6
DNA methylation of transcript factors and steroidogenic genes promoters in adrenal glands of pullets. a) Schematic diagram showing the amplified segments (S) on the promoter sequence of SF-1. b) DNA methylation status on the promoter of SF-1; c) Schematic diagram showing the amplified CREB; d) DNA methylation status on the promoter of CREB. e) Schematic diagram showing the amplified segments (S) on the promoter sequence of SREBP1. f) DNA methylation status on the promoter of SREBP1; g) Schematic diagram showing the amplified CYP11A1; h) DNA methylation status on the promoter of CYP11A1.; i) Schematic diagram showing the amplified CYPA2(S); j) DNA methylation status on the promoter of CYP21A2. Values are means ± SEM, *P < 0.05, compared with control (n = 3)
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