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A single-cell assessment of intramuscular and subcutaneous adipose tissue in beef cattle 

ABSTRACT: Intramuscular fat (IM; marbling) deposition is the deciding factor of beef quality grade in the U.S. Defining molecular mechanisms regulating adipogenesis in distinct anatomical areas in beef cattle is key to the development of strategies for marbling enhancement while limiting accumulation of excess subcutaneous adipose tissue (SAT; backfat). Our objective was to define the IM and SAT transcriptional heterogeneity at the whole tissue and single-cell levels in beef cattle. Longissimus dorsi muscle (9-11th rib) samples were collected from two harvested finished beef steers to dissect matched IM and adjacent SAT. Nuclei were isolated by dounce homogenization, then sequenced via bulk RNA sequencing (RNAseq) and single-nuclei RNA sequencing (snRNAseq) with 10x Genomics in an Illumina NovaSeq 6000. Analysis was conducted via Cell Ranger pipeline and Seurat in R Studio. By the expression of signature marker genes, snRNAseq analysis identified mature adipocytes (AD; ADIPOQ, LEP), adipose stromal and progenitor cells (ASPC; PDGFRA), endothelial cells (EC; VWF, PECAM1), smooth muscle cells (SMC; NOTCH3, MYL9) and immune cells (IMC; CD163, MRC1). We detected six cell clusters in SAT and nine in IM. Across IM and SAT, AD was the most abundant cell type, followed by ASPC, SMC, and IMC. In SAT, AD made up 50% of the cellular population, followed by ASPC (31%), EC (14%), IMC (1%), and SMC (4%). In IM depot, AD made up 23% of the cellular population, followed by ASPC with 19% of the population, EC with 28%, IMC with 7% and SMC with 12%. The abundance of ASPC and AD was lower in IM vs. SAT, while IMC was increased, suggesting a potential involvement of immune cells on IM deposition. Accordingly, both bulk RNAseq and snRNAseq analyses identified activated pathways of inflammation and metabolic function in IM. These results demonstrate distinct transcriptional cellular heterogeneity between SAT and IM depots in beef cattle, which may underly the mechanisms by which fat deposits in each depot. The identification of depot-specific cell populations in IM and SAT via snRNAseq analysis has the potential to reveal target genes for the modulation of fat deposition in beef cattle.

ORGANISM(S): Bos taurus

PROVIDER: GSE302935 | GEO | 2025/07/31

REPOSITORIES: GEO

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Project description:Adipose tissue plays a central role in regulating whole-body metabolic health, facilitated by the variety of cell types and their wide-ranging functions. In addition, depot-specific differences in adipose tissue have been shown to play important roles in different disease states including obesity, diabetes, and metabolic dysfunction in human and animal models. For early postpartum dairy cattle, metabolic dysfunction, triggered by a negative energy balance, is often manifested as subclinical ketosis (SCK). However, the role that subcutaneous (SAT) and visceral (VAT) adipose tissue depots, and their diverse cellular compositions, play in the response to subclinical ketosis conditions is unclear. Flank SAT and omental VAT were collected via laparotomy from five non-ketotic (NK; BHB ≤ 0.8 mmol/L) and five subclinical ketosis (SCK; 1.4 mmol/L < BHB ≤ 2.6 mmol/L) multiparous cows during early lactation. Following collection, nuclei were isolated from the tissue and subjected to single-nuclei RNA sequencing in order to investigate the transcriptional cellular heterogeneity. Distinct clusters of adipocytes (AD), adipose stem/progenitor cells (ASPC), immune cells (IMC), endothelial cells (EC), and pericyte/smooth muscle cells (PE/SMC) were identified in both adipose depots, with a greater abundance of ASPC in SAT compared to VAT. In addition, we identified a VAT-specific AD subtype characterized by higher expression of progenitor-like marker genes. While the abundance of none of the identified cell subtypes were different between SCK and NK, underlying transcriptional changes provided insight into potential effects of SCK. In general, SCK was associated with pro-lipogenic, anti-inflammatory, and pro-angiogenic transcriptional changes, possibly indicating a greater capacity for homeostatic responsiveness in SAT under conditions of enhanced negative energy balance. In contrast, SCK appeared to promote transcriptional changes indicative of impaired adipogenesis, impaired angiogenesis, and increased inflammation in VAT. Uniquely, our study presents novel insight into the cellular heterogeneity of adipose tissue in dairy cattle with subclinical ketosis. Furthering our understanding of the role of adipose tissue in response to this form of metabolic challenge has the potential to enhance efforts aimed at limiting the incidence and impact of subclinical ketosis and improving the health and productivity of dairy cattle.

Project description:*Background: Adipocytes mainly function as energy storage and endocrine cells. The amount and distribution of fat are important factor that influence the meat quality in the beef industry. Fat depot can be found around internal organ (ometal), beneath the skin (subcutaneous), and between muscles (intramuscular). Different adipose depot showed the biological and genetic difference depending on their location. This inter-depot variation might be influenced by the inherent genetic programing for development of adipose depots. In this study, we used RNA-seq data to investigate the difference in transcriptome of various adipose depots in Hanwoo. *Results: Using RNA-seq, we identified 5797, 2156, and 5455 DEGs in the comparison between OI, OS, and IS respectively (FDR<0.01) and found 853, 48, and 979 DEGs specific to subcutaneous, intramuscular and omental fat respectively. DEGs in intramuscular fat were highly enriched the metabolism related pathways compared to other fat depots. DEGs specific to the omental fat is significantly enriched in PPAR signaling pathway and cell-junction related pathway. In subcutaneous fat, cytokine-cytokine receptor interaction with chemokines (CXC and CC subfamily) was the most significantly enriched the pathways. Interestingly, melanogenesis pathway was associated with the subcutaneous depot. Even though the adipose tissues shared the same pathways for adipocyte differentiation, the regulation of genes were different based on the depot. *Conclusions: We comparatively analyzed the transcripome profile from different adipose tissues using NGS and identified DEGs between adipose depot and specific to depot in Hanwoo animals. The functional annotation analysis of DEGs found that transcriptome profile difference in various adipose tissue of intramuscular, subcutaneous, and ometal fat. whole mRNA sequencing profiles of nine Korean native cattle (nine profiles of omental fat tissue, nine profiles of intramuscular fat tissue, nine profiles of subcutaneous fat tissue and eight profiles of muscle tissue)

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A single-cell assessment of intramuscular and subcutaneous adipose tissue in beef cattle

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