Elsevier

Gene

Volume 537, Issue 1, 1 March 2014, Pages 120-125
Gene

Expression profiles of key transcription factors involved in lipid metabolism in Beijing-You chickens

https://doi.org/10.1016/j.gene.2013.07.109Get rights and content

Highlights

  • Accumulation of IMF in breast and thigh from 8 to 14 wk exceeded that from 14 to 20 wk.

  • C/EBPα and PPARγ were important effectors in lipid metabolism in chickens.

  • C/EBPβ might play a role in IMF deposition in the early developmental stages.

  • PPARα in breast and thigh muscle was significantly higher than that in abdominal fat.

Abstract

Intramuscular fat (IMF) is a crucial factor for the meat quality of chickens. With the aim of studying the molecular mechanisms underlying IMF deposition in chickens, the expression profiles of five candidate transcription factors involved in lipid metabolism in several tissues were examined in Beijing-You (BJY) chickens at five ages (0, 4, 8, 14 and 20 wk). Results showed that accumulation of IMF in breast (IMFbr), thigh (IMFth) and abdominal fat weight 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 of IMFbr. As for the expression profiles of key transcription factors: 1) expression of C/EBPα and PPARγ in abdominal fat was significantly higher than that in breast and thigh muscles at all ages. The expression of C/EBPα was positively correlated with PPARγ in both breast and thigh muscles, which indicated that both C/EBPα and PPARγ promoted fat deposition and might act through a unified pathway; 2) the expression of SREBP-1 in 0, 4, and 8 wk in thigh muscle was significantly higher than that in breast; 3) expression of C/EBPβ at 4 and 8 wk was significantly higher than that at 14 and 20 wk; and it was positively correlated with IMFth and IMFbr from 0 to 8 wk; 4) expression of PPARα in breast and thigh muscles was significantly higher than that in abdominal fat. Taken together, all five transcription factors studied play roles in lipid metabolism in chickens with C/EBPα and PPARγ being important effectors.

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).

References (37)

  • D.M. Muoio

    Fatty Acid Homeostasis and Induction of Lipid Regulatory Genes in Skeletal Muscles of Peroxisome Proliferator-activated Receptor (PPAR) α Knock-out Mice EVIDENCE FOR COMPENSATORY REGULATION BY PPARδ

    J. Biol. Chem.

    (2002)
  • M. Sekiya

    SREBP-1-independent regulation of lipogenic gene expression in adipocytes

    J. Lipid Res.

    (2007)
  • J.M. Ye

    Peroxisome Proliferator—Activated Receptor (PPAR)-α Activation Lowers Muscle Lipids and Improves Insulin Sensitivity in High Fat—Fed Rats Comparison with PPAR-γ Activation

    Diabetes

    (2001)
  • S. Zerehdaran et al.

    Estimation of genetic parameters for fat deposition and carcass traits in broilers

    Poult. Sci.

    (2004)
  • O. Barbier

    Pleiotropic actions of peroxisome proliferator–activated receptors in lipid metabolism and atherosclerosis

    Arterioscler. Thromb. Vasc. Biol.

    (2002)
  • G. Castillo

    Role and regulation of PPARγ during adipogenesis

    J. Anim. Sci.

    (1999)
  • Yongsheng Chang

    Keratinocyte Growth Factor Induces Lipogenesis in Alveolar Type II Cells through a Sterol Regulatory Element Binding Protein-1c–Dependent Pathway

    Am. J. Respir. Cell Mol. Biol.

    (2006)
  • Raghunath Chatterjee

    Suppression of the C/EBP family of transcription factors in adipose tissue causes lipodystrophy

    J. Mol. Endocrinol.

    (2011)
  • Cited by (18)

    • Label-free proteomic analysis reveals the differentiation between unfertilized and fertilized Beijing-You chicken eggs

      2020, International Journal of Biological Macromolecules
      Citation Excerpt :

      Beijing-You chicken is a traditional Chinese local variety in Beijing district, with a high fat content and an excellent flavor [8]. The Beijing-You chicken produces high quality meat and egg, and the egg is increasingly favored by consumers [9–11]. Proteomic research is accelerated by methodological developments in mass spectrometry and has increased the identification of new chicken egg proteins [12,13].

    • Gene expression and plasma lipid content in relation to intramuscular fat in Chinese indigenous Wuhua chicken

      2017, Journal of Applied Poultry Research
      Citation Excerpt :

      Ayers et al. [13] reported that A-FABP shuttling could maintain transcriptional activation of peroxisome proliferator-activated receptor-γ (PPARγ) to play important roles in lipid metabolism and adipocyte differentiation. In chickens, several other genes also have been demonstrated to be involved in the regulation of adipocyte differentiation and deposition, such as fatty acid synthetase (FAS), PPAR-γ, and apolipoprotein B (ApoB) [14, 15]. However, expression levels of A-FABP and other related genes in muscle fiber associated with IMF profile in slow growing breeds have been seldomly reported.

    View all citing articles on Scopus
    1

    The authors contributed equally to this work.

    View full text