Effect of starter diet supplementation on rumen epithelial morphology and expression of genes involved in cell proliferation and metabolism in pre-weaned lambs

Abstract

Starter feeding is usually used in lamb production to improve rumen development and to facilitate the weaning process, but molecular mechanism of which is not well understood. Therefore, the objective of this study is to investigate the effect of starter feeding on the expression of ruminal epithelial genes involved in cell proliferation, apoptosis and metabolism in pre-weaned lambs. We selected eight pairs of 10-day-old lamb twins. One twin was fed ewe milk (M, n=8), while the other was fed ewe milk plus starter (M+S, n=8). The lambs were sacrificed at 56 days age. Results showed that the lambs fed M+S had lower pH in the rumen and a higher concentration of acetate, propionate, butyrate and total volatile fatty acid (VFA). Compared with the M group, the concentration of β-hydroxybutyric acid in plasma had an increased trend, and the concentration of IGF-1 in plasma had an decreased trend in the M+S group. The length, width and surface of rumen papillae increased in the M+S group compared with the M group; this was associated with increased cell layers in the stratum corneum, stratum granulosum and total epithelia. Messenger RNA (mRNA) expression of proliferative genes of cyclin A, cyclin D1 and cyclin-dependent kinase 2 in the ruminal epithelia of M+S lambs was increased compared with M only lambs. The mRNA expression of apoptosis genes of caspase-3, caspase-8, B-cell lymphoma-2 (Bcl-2) and Bcl-2-associated X protein (Bax) in the M+S group was decreased compared with M group, but the ratio of Bcl-2 to Bax were not changed between the two groups. Expression of IGF-1 mRNA was decreased, but the mRNA expression of IGF-1 receptor was higher in ruminal epithelia in the M+S group. Furthermore, the mRNA expression of VFA absorption and metabolism genes of β-hydroxybutyrate dehydrogenase isoforms 1 and 3-hydroxy-3-methylglutaryl-CoA lyase had an increased trend in the M+S group than in the M group, but the mRNA expression of 3-hydroxy-3-methylglutaryl-CoA synthase isoform 1, monocarboxylate transporter isoform 1 and putative anion transporter isoform 1 had a decreased trend in the M+S group than in the M group. These results suggest that starter feeding increased proliferation and inhibited apoptosis of ruminal epithelial cells, and may promote the VFA metabolism in ruminal epithelium in pre-weaned lambs. These findings provide new insights into improving rumen development by nutritional intervention strategies in pre-weaned lambs.

Growth of rumen papillae in weaned calves is associated with lower expression of insulin‐like growth factor‐binding proteins 2, 3, and 6

“…IGF-I directly regulates cell proliferation in cultured rumen epithelial cells of lambs (Baldwin, 1999). Gene expression of IGF-I in rumen papillae was lower in lambs fed milk and starter diet than in lambs fed milk only, while the expression of IGF-IR and length of rumen papillae were higher in the first than in the latter (Sun, Mao, Zhu, & Liu, 2018 Our previous study suggested that IGFBP5 was upregulated by weaning and might be necessary for the proliferation of rumen epithelial cells of Japanese Black calves (Nishihara et al, 2018).…”

“…IGF‐I directly regulates cell proliferation in cultured rumen epithelial cells of lambs (Baldwin, ). Gene expression of IGF‐I in rumen papillae was lower in lambs fed milk and starter diet than in lambs fed milk only, while the expression of IGF‐IR and length of rumen papillae were higher in the first than in the latter (Sun, Mao, Zhu, & Liu, ). However, there were no changes in the expressions of IGF genes and corresponding receptor genes in the Holstein calves examined in the present study, indicating that IGFs and their receptors have no direct effects on the growth of rumen papillae.…”

Effect of Different Energy Levels in Starter Ration Of Suckling Angus Calves on Blood Biochemical Parameters, Hormone Profile, Immune Response and Antioxidant Status

“…Adequate amount of forage and starter diet fosters rumen volume and papillae development, favoring growth of pre-weaned calves. Sun et al (2018) reported that starter feeding increased proliferation of rumen and enhanced rumen development in pre-weaned lambs. Composition of solid feed during preweaning stage could also affect rumen development, growth and behavior of animals (Suárez et al, 2006;Khan et al, 2008;Muhammad et al, 2016;Aziz ur Rahman et al, 2017;Rahman et al, 2019).…”

Early solid diet supplementation influences proteomic of rumen epithelium in goat kids

“…As we know, the introduction of solid diets in early life was a vital driver for the development of rumen epithelium due to the nutrient components in solid diet [3]. Previous studies found that supplementing solid feed during pre-weaning period can effectively increase rumen weight and papillae size, enhance the physical barrier of rumen to harmful substances, and ultimately have a positive effect on the health and growth of young ruminants [4][5][6]. Other studies reported that early feeding starter can influence gene expression of rumen epithelium in lambs and sheep, for example, down-regulated genes including IL-6, IL-10, and IFN-γ [7]and up-regulated genes containing MCT1, MCT4 and NHE3 [8].…”