The periparturient period is associated with structural and transcriptomic adaptations of rumen papillae in dairy cattle

Abstract

The structural and functional adaption of the rumen epithelium during the transition period is largely undescribed. To characterize the adaptation of the rumen epithelium during transition, multiparous dairy cattle (n=12) fitted with rumen fistulas and fed a low-energy dry cow diet (1.37 Mcal/kg, net energy for lactation) were transitioned abruptly to a high-energy lactating cow diet (1.68 Mcal/kg, net energy for lactation) immediately after parturition. Rumen papillae were biopsied at -3, +1, and +6 wk relative to calving. The histology of morphology of the rumen papillae was evaluated under the light microscope and electron microscope, and mRNA profiling was performed using an Affymetrix GeneChip Bovine Gene 1.0 ST Array (Affymetrix, Santa Clara, CA). Data preprocessing was conducted using the robust multi-array average method, and detection of significant genes was conducted using ANOVA. Also, the Benjamini-Hochberg false discovery rate of 0.1 was applied. Microscopic examination of rumen papillae revealed an increase in epithelial desquamation during early lactation as sloughing scores increased from 1.7 ± 0.2 at -3 wk to 4.1 ± 0.3 and 3.4 ± 0.2 at +1 and + 6 wk, respectively. A total of 1,011 (-3 vs. +1 wk) and 729 (-3 vs. +6 wk) differentially expressed genes were identified (false discovery rate of 0.10, P<10(-3), fold-change ± 1.2 cut-off). A group of differentially expressed genes involved in desmosome assembly (DSG1, CDSN), epidermal growth factor signaling (EGFR, EREG), transforming growth factor β signaling (TGFB1), and the insulin-like growth factor-axis (GHR, IGFBP2, IGFBP3, CTGF) was also validated using PCR. Gene network analysis found that EGFR, GHR, and TGFB1 were focal points of the top pathways, thereby supporting the importance of these regulatory genes to the adaptive response of rumen papillae in early lactation. The microscopic and transcriptomic changes in this study provide insight into the mechanisms responsible for the rapid rate of cellular and molecular adaptations of rumen papillae tissue during the transition period in dairy cattle. In conclusion, the experimental data support the hypothesis that rumen papillae adapt in early lactation by altering their gene expression patterns and, thus, their epithelial structure.

Abundance of ruminal bacteria, epithelial gene expression, and systemic biomarkers of metabolism and inflammation are altered during the peripartal period in dairy cows

“…The results for TGFB1 and EREG agree with the recent study by Steele et al (2015) using a similar experimental timeline. However, the finding of an upregulation of EGFR, a member of the epidermal growth factor family (Shirakata et al, 2000), at the end of the peripartal period is opposite to the observation by Steele et al (2015). An upregulation of EREG expression can induce autocrine growth factors leading to greater keratinocyte differentiation (Shirakata et al, 2000).…”

“…The present data support a role for TGFB1 in the regulation of growth and differentiation of rumen epithelium in early lactation (Connor et al, 2014;Steele et al, 2015). The TGFB1 protein mediates several physiological processes, including inhibition of cell proliferation, activation of apoptosis, and cellular differentiation (Massagué et al, 2000;Moustakas et al, 2002).…”

“…Understanding ruminal epithelium physiology during transition will help nutritionists to develop strategies to enhance dairy cow health and production in early lactation (Steele et al, 2015). Several processes involved in ruminal epithelium adaptations to degree of diet fermentability are closely related to the production of VFA, especially butyrate (Sakata and Tamate, 1978;Sakata and Yajima, 1984).…”

“…Using microscopy, Steele et al (2015) reported morphological changes in the ruminal epithelium after calving without changes in mRNA expression of cell adhesion proteins (Steele et al, 2015). In a recent study, Liu et al (2013) reported that a high-grain diet in goats caused massive disruption of ruminal epithelial TJ with profound alterations in ruminal epithelial structure and changes in TJ protein expression, in particular claudin-4, occludin, and TJP1.…”

“…However, evidence also points at mRNA expression and transporter and enzyme activity in the initial response driving epithelial cell function . Few studies have investigated the molecular adaptations of ruminal epithelium during the peripartum period (Dionissopoulos et al, 2014;Steele et al, 2015). These studies revealed the existence of interactions among genes of the immune system and those involved in the preparation for the onset of lactation (Dionissopoulos et al, 2014), as well as the presence of growth factors that seem to be regulated after parturition (Steele et al, 2015).…”