Longitudinal muscle gene expression patterns associated with differential intramuscular fat in cattle

Abstract

Intramuscular fat (IMF) can improve meat product quality through its impact on flavour and juiciness. High marbling cuts can command premium prices in some countries and grading systems, but there is substantial cost involved in choosing to grain feed animals in an effort to deposit more IMF. There would be value in developing methods to predict predisposition to 'marble' well. Unfortunately, the biological mechanisms underpinning marbling remain a mystery: the key adipocyte cell populations have not been defined, there are no reliable DNA markers, no known (if any) causal mutations and gene expression analyses in the main have tended to characterise increases in expression of end-point fat metabolism proteins such as the fatty acid-binding proteins. To shed light on expression-based markers of marbling potential, we contrasted LD gene expression in high IMF Wagyu cross animals with a low IMF Piedmontese cross at various time points. The expected divergence in the fat metabolism genes FABP4, THRSP, CIDEC and ACACA between the breeds occurs surprisingly late in postnatal development at about 20 months. On the other hand, divergent expression of WISP2, RAI14 and CYP4F2 was discovered in animals at or before 12 months of age, suggesting these genes may have potential as earlier predictors of marbling potential. In line with other researchers, we found intriguing links between IMF development and connective tissue remodelling. WISP2 -a novel adipokine highly expressed and secreted by adipose precursor cells and an inhibitor of the pro-fibrotic connective tissue growth factor -emerges as a particularly attractive candidate. It is relatively upregulated in high marbling Wagyu before admission to feedlotting, somewhere between 7 and 12 months. This difference is subsequently maintained until 25 months, but not thereafter. RAI14, thought to play a role in porcine adipocyte differentiation and with links to retinoic acid metabolism, has an unusual expression profile. Its expression level increases monotonically with postnatal development, and is always higher in Wagyu than Piedmontese. Strong, sustained upregulation of the anti-inflammatory CYP4F2 in Piedmontese is consistent with Wagyu adiposity being a pro-inflammatory state. Application of regulatory impact factor analysis, a network method for identifying causal effector molecules, suggests marbling roles for transcription factors previously implicated in (1) the formation of liposarcoma (unconstrained fatty masses) (YEATS4, MDM2), (2) adipogenesis (CREBL2, SP1, STAT1) and (3) inflammation (ISGF3G, HOXB13, PML).

Increased expression of thyroid hormone responsive protein (THRSP) is the result but not the cause of higher intramuscular fat content in cattle

“…Higher mRNA abundance of THRSP in MLD was also found in our study in F 2 ‐bulls (Charolais × Holstein) with high IMF compared to those with low IMF 25, 26. Several experiments in cattle indicated that THRSP mRNA expression increases with age of the animals and is affected by diet and age of weaning 19, 27, 28. In all of these studies, THRSP mRNA was measured in samples of MLD comprising different amounts of intramuscular fat cells beside other cell types.…”

“…However, the underlying molecular mechanisms determining fat storage and distribution are widely unknown 14. Consequently, the identification and characterization of candidates for IMF deposition in cattle have been in the focus of numerous studies 15-19. The gene encoding THRSP was repeatedly named a candidate for different IMF in MLD and an important regulator of adipogenesis and lipogenesis in cattle 17, 19-24.…”

Review: Animal model and the current understanding of molecule dynamics of adipogenesis

“…Previous studies have suggested that the high deposition of IMF in Wagyu is related to the differential expression of specific genes (Hudson et al, 2014). In most cattle breeds, IMF is first visible at about 11 months, with the greatest increases between 15 and 24 months.…”

“…Marbling is an important component of livestock production, as it is a major factor in the overall meat quality (flavor and tenderness), nutrition (protein and fat levels and fatty acid composition) and economic value (Pena et al, 2013;Hudson et al, 2014;Sadkowski et al, 2014). An increase in IMF has been proposed to occur either through the myogenic transdifferentiation of myogenic stem cells (MSC) in skeletal muscle through a complex regulatory pathway, which remains unclear, or through the multi-step process of adipogenic determination and differentiation of fibroblastlike preadipocytes into mature adipocytes assimilating lipid .…”

Genetic polymorphism analysis of 5' untranslated region of thyroglobulin gene in Bali cattle (Bos javanicus) from three different regions of Indonesia

“…Intramuscular fat (IMF) or also called as marbling has been studied contributed to the beef palatability or eating quality of beef through its attributes such as flavour, juiciness and tenderness (Okumura et al, 2007;Hudson et al, 2015), even though several studies showed that the association between marbling score and beef palatability attributes was a positively small (Wheeler et al, 1994;Platter et al, 2003). However, marbling score has been used as one of major determinants for beef palatability in international markets especially in Japan, Australia and USA (Watson et al, 2008;Gotoh et al, 2014).…”