A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats

Liu, Junhua; Xu, Tingting; Liu, Yujie; Zhu, Weiyun; Mao, Shengyong

doi:10.1152/ajpregu.00068.2013

Cited by 158 publications

(190 citation statements)

References 42 publications

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“…Prior to the current study, only one experiment has shown that cell adhesion genes are regulated in the RE. Liu et al (2013) reported that the transition from low to high energy diets is linked to the downregulation of CLDN 1, 4, and occludin, yet the expression of these genes in the current study was not affected. Two of the largest fold changes in both microarray comparisons in the current study were for desmoglein 1 (DSG1) and corneodesmosin (CDSN)-both desmosomal cadherins in the stratum granulosum and corneum of stratified squamous epithelium (SSE; Green and Jones, 1996).…”

contrasting

confidence: 56%

“…During the onset of ruminal acidosis, the structural integrity of the RE is compromised (Steele et al, 2011a), which is linked to the differential expression of various structural and SCFA metabolism genes (Penner et al, 2011;Steele et al, 2011b). In particular, genes associated with desmosomes (Steele et al, 2011a) and claudins (Liu et al, 2013) that are responsible for cellular adhesion have been differentially expressed in ruminants during high grain feeding. During ruminal acidosis, the structure of the RE can be compromised causing a pathological state; however, it is not known if similar changes occur due to the concert of dietary, physiologic, and metabolic changes in early lactation.…”

Section: Introductionmentioning

confidence: 99%

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

Steele

Schiestel

AlZahal

et al. 2015

Journal of Dairy Science

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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.

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contrasting

confidence: 56%

Section: Introductionmentioning

confidence: 99%

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

Steele

Schiestel

AlZahal

et al. 2015

Journal of Dairy Science

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“…The primers of cytokine (Liu et al, 2013), TLR (Charavaryamath et al, 2011), and glyceraldehyde-3-phosphate dehydrogenase (GAPDH; Wang et al, 2009) genes used in the present study were described in previous studies. All of the primer sequences are listed in Table S1.…”

Section: Methodsmentioning

confidence: 99%

Starter Feeding Supplementation Alters Colonic Mucosal Bacterial Communities and Modulates Mucosal Immune Homeostasis in Newborn Lambs

Liu

Bian²,

Sun

et al. 2017

Front. Microbiol.

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This study aims to investigate the effect of starter feeding supplementation on colonic mucosal bacterial communities and on mucosal immune homeostasis in pre-weaned lambs. We selected eight pairs of 10-day-old lamb twins. One twin was fed breast milk (M, n = 8), while the other was fed breast milk plus starter (M+S, n = 8). The lambs were sacrificed at 56 days age. Colonic content was collected to determine the pH and the concentrations of volatile fatty acids (VFA) and lactate. The colonic mucosa was harvested to characterize the bacterial communities using Illumina MiSeq sequencing and to determine mRNA expression levels of cytokines and toll-like receptors (TLR) using quantitative real-time PCR. The results show that starter feeding decreased luminal pH and increased the concentrations of acetate, propionate, butyrate, total VFA, and lactate in the colon. The principal coordinate analysis (PCA) and analysis of molecular variance show that starter feeding supplementation significantly affected the colonic mucosal bacterial communities with a higher relative abundance of the dominant taxa unclassified S24-7, Oscillibacter, Prevotella, Parabacteroides, Bifidobacterium, Ruminobacter, and Succinivibrio, and a lower proportion of unclassified Ruminococcaceae, RC9_gut_group, Blautia, Phocaeicola, Phascolarctobacterium, unclassified BS11_gut_group, unclassified family_XIII, and Campylobacter in lambs. Meanwhile, starter feeding decreased mRNA expression of TLR4 and cytokines TNF-α and IFN-γ in colonic tissue. Furthermore, the changes in the colonic mucosal mRNA expression of TLR and cytokines were associated with changes in mucosal bacterial composition. These findings may provide new insights into colonic mucosal bacteria and immune homeostasis in developing lambs.

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“…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. Our results suggest that during the transition period the ruminal epithelium experiences a slight impairment of barrier function.…”

Section: Gene Expression In Ruminal Epithelium During Transitionmentioning

confidence: 99%

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

Minuti

Palladino

Khan

et al. 2015

Journal of Dairy Science

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Seven multiparous Holstein cows with a ruminal fistula were used to investigate the changes in rumen microbiota, gene expression of the ruminal epithelium, and blood biomarkers of metabolism and inflammation during the transition period. Samples of ruminal digesta, biopsies of ruminal epithelium, and blood were obtained during -14 through 28d in milk (DIM). A total of 35 genes associated with metabolism, transport, inflammation, and signaling were evaluated by quantitative reverse transcription-PCR. Among metabolic-related genes, expression of HMGCS2 increased gradually from -14 to a peak at 28 DIM, underscoring its central role in epithelial ketogenesis. The decrease of glucose and the increase of nonesterified fatty acids and β-hydroxybutyrate in the blood after calving confirmed the state of negative energy balance. Similarly, increases in bilirubin and decreases in albumin concentrations after calving were indicative of alterations in liver function and inflammation. Despite those systemic signs, lower postpartal expression of TLR2, TLR4, CD45, and NFKB1 indicated the absence of inflammation within the epithelium. Alternatively, these could reflect an adaptation to react against inducers of the immune system arising in the rumen (e.g., bacterial endotoxins). The downregulation of RXRA, INSR, and RPS6KB1 between -14 and 10 DIM indicated a possible increase in insulin resistance. However, the upregulation of IRS1 during the same time frame could serve to restore sensitivity to insulin of the epithelium as a way to preserve its proliferative capacity. The upregulation of TGFB1 from -14 and 10 DIM coupled with upregulation of both EGFR and EREG from 10 to 28 DIM indicated the existence of 2 waves of epithelial proliferation. However, the downregulation of TGFBR1 from -14 through 28 DIM indicated some degree of cell proliferation arrest. The downregulation of OCLN and TJP1 from -14 to 10 DIM indicated a loss of tight-junction integrity. The gradual upregulation of membrane transporters MCT1 and UTB to peak levels at 28 DIM reflected the higher intake and fermentability of the lactation diet. In addition, those changes in the diet after calving resulted in an increase of butyrate and a decrease of ruminal pH and acetate, which partly explain the increase of Anaerovibrio lipolytica, Prevotella bryantii, and Megasphaera elsdenii and the decrease of fibrolytic bacteria (Fibrobacter succinogenes, Butyrivibrio proteoclasticus). Overall, these multitier changes revealed important features associated with the transition into lactation. Alterations in ruminal epithelium gene expression could be driven by nutrient intake-induced changes in microbes; microbial metabolism; and the systemic metabolic, hormonal, and immune changes. Understanding causes and mechanisms driving the interaction among ruminal bacteria and host immunometabolic responses merits further study.

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A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats

Cited by 158 publications

References 42 publications

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

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

Starter Feeding Supplementation Alters Colonic Mucosal Bacterial Communities and Modulates Mucosal Immune Homeostasis in Newborn Lambs

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

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