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

Nishihara, Koki; Suzuki, Yutaka; Kim, Dahye; Roh, Sanggun

doi:10.1111/asj.13270

Cited by 12 publications

(14 citation statements)

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“…We observed that the IGFBP3 + EC appeared only in newborn calves considered to be functionally monogastric animals. The IGFBP3 encodes a protein that is known to inhibit the role of IGFs in cell proliferation [ 58 ]. This indicates that the disappearance of IGFBP3 + EC may facilitate the rumen epithelium development.…”

Section: Discussionmentioning

confidence: 99%

Microbiota-host crosstalk in the newborn and adult rumen at single-cell resolution

Zhu

Tang

et al. 2022

BMC Biol

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Background The rumen is the hallmark organ of ruminants, playing a vital role in their nutrition and providing products for humans. In newborn suckling ruminants milk bypasses the rumen, while in adults this first chamber of the forestomach has developed to become the principal site of microbial fermentation of plant fibers. With the advent of single-cell transcriptomics, it is now possible to study the underlying cell composition of rumen tissues and investigate how this relates the development of mutualistic symbiosis between the rumen and its epithelium-attached microbes. Results We constructed a comprehensive cell landscape of the rumen epithelium, based on single-cell RNA sequencing of 49,689 high-quality single cells from newborn and adult rumen tissues. Our single-cell analysis identified six immune cell subtypes and seventeen non-immune cell subtypes of the rumen. On performing cross-species analysis of orthologous genes expressed in epithelial cells of cattle rumen and the human stomach and skin, we observed that the species difference overrides any cross-species cell-type similarity. Comparing adult with newborn cattle samples, we found fewer epithelial cell subtypes and more abundant immune cells, dominated by T helper type 17 cells in the rumen tissue of adult cattle. In newborns, there were more fibroblasts and myofibroblasts, an IGFBP3+ epithelial cell subtype not seen in adults, while dendritic cells were the most prevalent immune cell subtype. Metabolism-related functions and the oxidation-reduction process were significantly upregulated in adult rumen epithelial cells. Using 16S rDNA sequencing, fluorescence in situ hybridization, and absolute quantitative real-time PCR, we found that epithelial Desulfovibrio was significantly enriched in the adult cattle. Integrating the microbiome and metabolome analysis of rumen tissues revealed a high co-occurrence probability of Desulfovibrio with pyridoxal in the adult cattle compared with newborn ones while the scRNA-seq data indicated a stronger ability of pyroxidal binding in the adult rumen epithelial cell subtypes. These findings indicate that Desulfovibrio and pyridoxal likely play important roles in maintaining redox balance in the adult rumen. Conclusions Our integrated multi-omics analysis provides novel insights into rumen development and function and may facilitate the future precision improvement of rumen function and milk/meat production in cattle.

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Section: Discussionmentioning

confidence: 99%

Microbiota-host crosstalk in the newborn and adult rumen at single-cell resolution

Zhu

Tang

et al. 2022

BMC Biol

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“…The fixed papillae samples were rinsed and dehydrated in a series of ethanol baths and then deparaffinized in xylene. Each papillae sample was stained with hematoxylin and eosin (H&E) and then observed under a Leica S9 Stereo microscope (Leica Microsystems Inc., Buffalo Grove, United States) as described previously ( Nishihara et al, 2019 ).…”

Section: Methodsmentioning

confidence: 99%

Effects of Heat Stress on the Ruminal Epithelial Barrier of Dairy Cows Revealed by Micromorphological Observation and Transcriptomic Analysis

et al. 2022

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Heat stress (HS) alters the rumen fermentation of dairy cows thereby affecting the metabolism of rumen papillae and thus the epithelial barrier function. The aim of the present study was to investigate if HS damages the barrier function of ruminal epithelia. Eight multiparous Holstein dairy cows with rumen cannula were randomly equally allocated to two replicates (n = 4), with each replicate being subjected to heat stress or thermal neutrality and pair-feeding in four environmental chambers. Micromorphological observation showed HS aggravated the shedding of the corneum and destroyed the physical barrier of the ruminal epithelium to a certain extent. Transcriptomics analysis of the rumen papillae revealed pathways associated with DNA replication and repair and amino acid metabolism were perturbated, the biological processes including sister chromatid segregation, etc. were up-regulated by HS, while the MAPK and NF-kB cell signaling pathways were downregulated. However, no heat stress-specific change in the expression of tight junction protein or TLR4 signaling was found, suggesting that HS negatively affected the physical barrier of the ruminal epithelium to some extent but did not break the ruminal epithelium. Heat stress invoked mechanisms to maintain the integrity of the rumen epithelial barrier by upregulating the expression of heat shock protein and repairments in rumen papillae. The increase in amino acid metabolism in rumen papillae might affect the nutrient utilization of the whole body. The findings of this study may inform future research to better understand how heat stress affects the physiology and productivity of lactating cows and the development of mitigation strategies.

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“…Therefore, it is possible that IGFBP might prevent BREC proliferation. Expression of IGFBP2 , IGFBP3 , and IGFBP6 in the rumen papillae of weaned calves was, respectively, 93%, 78%, and 85% lower than that in the rumen papillae of suckling calves (Nishihara et al., 2019). Therefore, we analyzed the effect of the IGFBP2 protein on BREC proliferation.…”

Section: Discussionmentioning

confidence: 99%

“…Gene expression analysis was performed by qRT‐PCR using SYBR ® Premix ExTaq™ II (Tli RNaseH Plus) (TaKaRa Bio) in a Thermal Cycler Dice ® Real Time System II (TaKaRa Bio). The primer sequences were described in our previous study (Nishihara et al., 2019); the PCR efficiencies were 0.8–1.2 for each primer pair, as determined by drawing standard curves using serial dilutions of pooled cDNAs. Beta actin (ACTB) and 18S were detected as reference genes.…”

Section: Methodsmentioning

confidence: 99%

“…Using comparative transcriptome analysis of rumen papillae in suckling and weaned calves, we previously showed that the gene expression levels of IGFBP2, IGFBP3, and IGFBP6 were lower in the rumen papillae of weaned calves than in those of suckling calves; however, there was no difference in the expression of IGFBP1 , IGFBP4, and IGFBP5 (Nishihara et al., 2018). In addition, the length of rumen papillae and the gene expression of IGFBP2 , IGFBP3 , and IGFBP6 were negatively correlated (Nishihara, Suzuki, Kim, & Roh, 2019). These findings suggest that low expression of IGFBP2 , IGFBP3 , and IGFBP6 might promote rumen epithelial cell proliferation and that the expression of these genes might be regulated by SCFA concentration, pH, ruminal metabolites such as lactate, and molecules derived from ruminal bacteria such as lipopolysaccharide (LPS).…”

Section: Introductionmentioning

confidence: 99%

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Ruminal epithelial insulin‐like growth factor‐binding proteins 2, 3, and 6 are associated with epithelial cell proliferation

Nishihara

Suzuki

Roh

2020

Animal Science Journal

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Jacobson, & Getty, 1962). The growth of rumen papillae increases the surface area of the rumen and the absorption of short-chain fatty acids (SCFAs: acetic acid, propionic acid, and butyric acid, among others). Therefore, understanding the mechanisms of growth of rumen papillae and rumen epithelial cells is important for devising strategies to improve ruminant productivity. Previously, it was shown that rumen papillae developed remarkably when the feed was changed from milk to roughage or a concentrated diet. The growth of rumen papillae was induced by SCFAs, and butyrate was the most potent activator of rumen papillae growth (Sakata & Tamate, 1978). However, the molecular mechanism regulating the growth of rumen papillae remains unclear. Six isoforms of insulin-like growth factor-binding protein (IGFBP) are known to regulate epithelial cell proliferation and differentiation in some tissues by controlling the activity of insulin-like growth factor I (IGF-I) or insulin-like growth factor II (IGF-II) (Firth & Baxter, 2002). For example, IGFBP4 bound to IGF-I in the small intestine of mice and prevented IGF-I binding to its receptors and cell proliferation (Austin, Imam, Pintar, & Brubaker, 2015). IGFBP2 prevented cell proliferation in human embryonic kidney fibroblasts and the small intestine (Corkins,

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

Cited by 12 publications

References 36 publications

Microbiota-host crosstalk in the newborn and adult rumen at single-cell resolution

Microbiota-host crosstalk in the newborn and adult rumen at single-cell resolution

Effects of Heat Stress on the Ruminal Epithelial Barrier of Dairy Cows Revealed by Micromorphological Observation and Transcriptomic Analysis

Ruminal epithelial insulin‐like growth factor‐binding proteins 2, 3, and 6 are associated with epithelial cell proliferation

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