Expression profiles of key transcription factors involved in lipid metabolism in Beijing-You chickens
Introduction
It is commonly known that intramuscular fat (IMF) contributes to flavor and juiciness. It is an important factor for the palatability of chicken meat. The content of IMF is the result of lipogenesis and lipolysis with complex molecular mechanisms. Chickens differ from mammals in having minimal dissectible adipose tissue associated with the connective elements of skeletal muscle and lipid accumulation is more influenced by uptake of blood lipids and subsequent lipogenesis rather than de novo fatty acid synthesis (Griffin et al., 1987, 1992). Liver serves as the main site of fatty acid synthesis and exports lipids as lipoproteins along with those derived from the gut (Griffin et al., 1987, 1992; Leclercq et al., 1984, Leveille et al., 1975). Together, these serve as substrates for use by other tissues, including deposition in muscle as well as in adipose tissue. The regulation of lipid deposition in adipose tissue is incompletely understood but can be expected to involve adipogenesis (differentiation and maturation), lipid transport, lipogenesis and lipolysis; the latter three would be of additional importance in muscle.
There is evidence, from a variety of species, for certain transcription factors playing roles in controlling adipocyte differentiation, lipogenesis and lipolysis (Haraguchi et al., 2003, Hausman et al., 2009, Hummasti et al., 2008). Adipogenesis is a well-regulated process controlled by a highly coordinated activation of various transcription factors. Temporal expression, in a highly coordinated cascade, of transcripts for CCAAT/enhancer-binding protein factors (C/EBPα, C/EBPβ), sterol regulatory element-binding protein 1 (SREBP1), and peroxisome proliferator-activated receptors (PPARα and PPARγ) is especially important (Elam et al., 2001, Koo et al., 2001, Rosen et al., 2000). SREBP1 plays an important role in the early stages of adipogenesis (Kim and Spiegelman, 1996). In addition to C/EBPβ being expressed in the early stages of adipogenesis (Darlington et al., 1998, Timchenko et al., 1996), C/EBPβ as a transcriptional relay might be under the direct control of some effects of insulin and/or SREBP1 in mature fat cells (Le Lay et al., 2002, Timchenko et al., 1996). Subsequently, C/EBPβ induces the expression of C/EBPα and PPARγ at later stages of cell differentiation (Rosen et al., 2002, Timchenko et al., 1996) and these participate in a positive feedback loop, promoting and maintaining the differentiated state (Yeh et al., 1995a). The two transcription factors, C/EBPα and PPARγ, play essential roles in activating terminal differentiation of adipocytes, lipid synthesis and other specific programs (Hausman et al., 2009, Olofsson et al., 2008, Rosen et al., 2002). PPARα is another important contributor to lipid metabolism by increasing fatty acid β-oxidative and lipid oxidation, hence reducing lipid accumulation (Muoio et al., 2002, Tsuchida et al., 2005, Ye et al., 2001).
The dynamics of these transcription factors (SREBP1, C/EBPβ, C/EBPα, PPARγ and PPARα) in important tissues across maturation in chickens are still unclear, as are the possible effects of the transcription factors on fat deposition. Beijing-You (BJY) chickens are a local variety, with a high fat content and an excellent flavor. The objective of this study was to describe developmental changes and explore possible relationships between expression of transcription factors and fat deposition in economically important tissues during growth of chickens.
Section snippets
Animals and sample collection
All experimental procedures were performed according to the Guidelines for Experimental Animals established by the Ministry of Science and Technology (Beijing, China). Fifty BJY male hatchlings came from conservation stock (Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China) and were randomly assigned to five groups, each of 10 birds. All birds were raised under recommended conditions with ad libitum feed and water.
At each age tested (day of hatch, 4, 8, 14
Content of IMF (%) in skeletal muscle and the weight of abdominal fat
The contents of IMFbr and IMFth at 4 wk were significantly higher than those at 8 wk (P < 0.01). All three variables increased significantly (P < 0.01) after 8 wk (Fig. 1). The accumulation of IMF from 8 to 14 wk exceeded that from 14 to 20 wk in both breast (1.46% vs 0.55%) and thigh (6.87% vs 2.40%). Additionally, at each age except 0 wk, IMFth was 4–7 times that of IMFbr.
The expression of transcription factors potentially related to IMF
Expression, in each tissue of interest and at the five ages, of the transcription factors (SREBP1, C/EBPβ, C/EBPα, PPARγ and PPARα)
Relationships between transcription factors and fat traits
Changes in the expression of C/EBPβ were positively correlated with IMFth (r = 0.62, P < 0.01) and with IMFbr only at 0 to 8 wk (r = 0.61, P = 0.01), but negatively correlated (r = − 0.69, P < 0.01) with abdominal fat weight (AbFW) from 4 to 20 wk. The expression of PPARα, just for weeks 0 to 8, was negatively correlated with IMFth (r = − 0.69, P < 0.01). Several other correlations, for part or all of the ages examined, existed but none exceeded 0.6 (positive or negative).
Associations among the five transcription factors
SREBP1 was positively correlated with PPARγ
The content of fat in different tissues and different growth stages
IMF is the main factor underlying tenderness, juiciness and flavor, and it changed with aging. In this study, IMFbr and AbFW at 20 wk were significantly higher than those at 14 wk and they were both notably higher than before 8 wk. IMFth at 14 and 20 wk was significantly higher than that at 4 and 8 wk. These results were consistent with Li et al.'s (2008) study. As Ye et al. (2009) reported, at each age except 0 wk, IMFth was 4–7 times that of IMFbr.
According to our finding that the increases in the
Conclusion
The current study has shown that accumulation of IMF in breast (IMFbr) and thigh (IMFth) and abdominal fat weight (AbFW) increased significantly (P < 0.01) after 8 wk; accumulation of both IMFbr and IMFth from 8 to 14 wk exceeded that from 14 to 20 wk; IMFth was 4–7 times that of IMFbr. Based on the expression profiles of key transcription factors, we found that 1) expression of both C/EBPα and PPARγ was consistent with their promoting fat deposition and might act through a unified pathway in
Conflict of interest
The authors do not have any possible conflicts of interest.
Acknowledgments
Authors acknowledged W. Bruce Currie (Emeritus Professor, Cornell University) for his contributions to the manuscript. The research was supported by grants from the National Natural Science Foundation of China (31272437), the National High-tech R&D Program (2013AA102501), and the China Agriculture Research System (CARS-42).
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The authors contributed equally to this work.