Adipose tissue transcriptional profile and extracellular matrix properties in beef cattle intramuscular, subcutaneous and visceral depots

Deposition of intramuscular adipose tissue (IMAT; marbling) is one of the primary determinants for beef quality grade within the U.S. However, IMAT accumulation is often secondary to subcutaneous (SCAT) and visceral (VIAT) adipose tissue deposition, which results in lower product yield. The mechanisms that underlie the differences in the accumulation of IMAT, SCAT, and VIAT are still not fully understood. The aim of this study was to define the depot-specific transcriptome and adipocyte function in IMAT, SCAT and VIAT in beef cattle. Functional transcriptome analysis indicated the activation of pathways for greater lipid accumulation and immune function in VIAT and SCAT compared with IMAT. Florescent activated cell sorting analysis identified a greater percentage of adipocyte stem and progenitor cells (ASPC) within IMAT compared to SCAT and VIAT, but lower ASPC’s proliferation in vitro, suggesting potential functional defects on IMAT’s adipogenic capacity. In vitro culture of adipocytes revealed greater lipid accumulation and insulin responses, and lower lipolysis of SCAT compared to IMAT adipocytes, with VIAT adipocytes having a characteristic of both SCAT, and IMAT adipocytes. Our findings revealed the depot-specific transcriptional profile of IMAT, SCAT and VIAT in beef cattle, which were corroborated by differences on adipocyte metabolic function in vitro. The extracellular matrix (ECM) is a collagenous scaffold that provides structure for adipose tissue (AT) growth and cellular function. In cattle, the deposition of intramuscular AT (marbling, IMAT) is desired, however, excessive amounts of both subcutaneous (SCAT) and visceral (VIAT) also accumulate, which result in increased losses as they are removed from the carcass as waste fat. Our study aimed to evaluate the ECM properties of IMAT, SCAT and VIAT in finished beef cattle and determine the depot-specific effects of ECM microenvironment on adipocyte function. IMAT and SCAT from the longissimus dorsi muscle (9-11th ribs) and VIAT from the greater omentum were collected from finished beef steers at harvest. AT samples were assessed for collagen content, collagen fibrillogenesis, adipocyte size, gene expression of ECM remodeling, and viscoelasticity (rheometer). Additionally, we aimed to culture preadipocytes within native decellularized ECM. Fat accumulation was increased in VIAT as frequency of adipocyte size was greater than IMAT and SCAT between 60-120µm, and IMAT at >120µm. Additionally, Total collagen content was greater in IMAT compared to SCAT and VIAT, analyzed using both hydroxyproline (p=0.0050) and picrosirius red (p=<0.0010), though collagen fibrillogenesis and stiffness measured by rheology were decreased in IMAT compared to SCAT. This suggests decreased collagen crosslinking in IMAT, and reduced protein turnover in SCAT and VIAT. Notably, IMAT had increased TIMP2 and LOX gene expression compared to SCAT, and decreased FN1 compared to VIAT suggesting increased ECM remodeling in IMAT. Adipocytes differentiated within decellularized muscle and AT responded differently to the ECM microenvironment. There was a greater expression of CEBPA, a marker of adipogenesis, in 3T3-L1 adipocytes cultured in SCAT and VIAT ECM compared to muscle, suggesting that muscle ECM may limit adipogenesis. Defining the characteristics of bovine AT ECM can aid in future discovery for modulating fat deposition and improving quality grades in beef cattle.

Embargo status: Restricted until 06/2027. To request the author grant access, click on the PDF link to the left.