Fat depot-specific differences in pref-1 gene expression and adipocyte cellularity between Wagyu and Holstein cattle

https://doi.org/10.1016/j.bbrc.2014.01.177Get rights and content

Highlights

  • Pref-1 mRNA expression in mesenteric fat was higher than subcutaneous fat.

  • Pref-1 mRNA expression in Holstein mesenteric fat was higher than Wagyu.

  • The mesenteric adipocyte size of Holstein was smaller than Wagyu.

Abstract

Preadipocyte factor-1 (pref-1) is specifically expressed in preadipocytes and acts as a gatekeeper of adipogenesis by maintaining the preadipocyte state and preventing adipocyte differentiation. We hypothesized that the breed differences of adipogenic capacity in cattle could be explained by the expression level of pref-1. In this experiment, we studied the expression level of the pref-1 gene and adipocyte cellularity in subcutaneous and mesenteric adipose tissues of Japanese Black (Wagyu) and Holstein fattening cattle. In subcutaneous adipose tissue, there were no significant differences in the pref-1 gene expression levels and adipocyte sizes between the breeds. In contrast, the expression level of the pref-1 gene in mesenteric adipose tissue of Holsteins was significantly higher than that of Wagyu. In addition, the size of mesenteric adipocytes in Holsteins was significantly smaller than that of Wagyu. These results indicate that the breed differences of fattening cattle affect the expression pattern of the pref-1 gene and adipocyte cellularity in a fat depot-specific manner.

Introduction

Adipose tissue growth (adipogenesis) is dependent on cellular events concerning both the differentiation of preadipocytes and the terminal differentiation of adipocytes [1]. Adipogenic transcription factors, the CCAAT/enhancer-binding protein (C/EBP) family (C/EBPα, C/EBPβ, and C/EBPδ) and the peroxisome proliferator-activated receptor γ2 (PPARγ2), play essential roles during adipogenesis [2], [3].

Preadipocyte factor-1 (pref-1) is a trans-membrane protein specifically expressed in preadipocytes [4], [5]. Pref-1 is a molecular gatekeeper of adipogenesis, which acts by maintaining the preadipocyte state and preventing adipocyte differentiation [6], [7]. Therefore, pref-1 expression has been used as a marker of the differentiation stage of adipogenesis and an indicator of preadipocyte density within adipose tissues [8], [9].

Beef breeds have been shown to have different capabilities for adipose tissue deposition. Japanese Black (Wagyu) cattle are characterized by the ability to accumulate higher amount of adipose tissues than Holsteins [10]. Previously, we indicated that the expression level of the C/EBP family in Wagyu adipocytes was significantly higher than in those of Holsteins [11]. A comparative in vitro study of bovine preadipocyte differentiation showed that the differentiation potential of preadipocytes in Wagyu is higher than in Holsteins [12]. Overexpression of pref-1 inhibits adipocyte differentiation and adipose tissue growth in mice [13]. These results suggest that, in addition to the expression level of adipogenic transcription factors in adipocytes, breed differences of adipogenic capacity could be explained by the expression level of pref-1 in preadipocytes. However, the effects of breed difference on the expression of the pref-1 in bovine adipogenesis are still unclear. The aim of the present study was to elucidate the effects of breed difference on the expression of the pref-1 gene in the adipose tissue of Wagyu and Holstein from various anatomical sites (subcutaneous and mesenteric).

Section snippets

Animals

The experimental design has been described in detail by Yamada et al. [11]. In brief, sixteen fattening steers (Wagyu (n = 8) and Holstein (n = 8), aged 19–24 months) were fed concentrate (88% total digestible nutrients and 12% crude protein) and orchard grass hay (56% total digestible nutrients and 8% crude protein) ad libitum from 10 months of age until they were slaughtered. Feeds were individually provided in each group. Adipose tissue samples from two types of fat tissues (subcutaneous and

Adipocyte cellularity

In subcutaneous adipose tissue, there was no difference in adipocyte cellularity between the breeds (Fig. 1). In contrast, the photomicrographs of osmium-fixed mesenteric adipocytes showed that larger sizes of adipocytes were more abundant in Wagyu than in Holsteins (Fig. 2A and B). As compared to the Holstein, the mesenteric adipocyte size distribution in Wagyu shifted toward larger diameters (Fig. 2C). The mean diameter of mesenteric adipocytes in Wagyu was significantly larger than that of

Discussion

In the present study, we showed that mesenteric adipose tissues expressed significantly higher pref-1 mRNA levels than did subcutaneous adipose tissues. Tchkonia et al. [16] showed that subcutaneous preadipocytes differentiated better than did visceral preadipocytes. Adams et al. [17] also showed that thiazolidinedione promotes adipogenesis of subcutaneous preadipocytes to a greater extent than preadipocytes derived from the visceral fat depots. Sweter et al. [18] indicated that the expression

Acknowledgments

This work was supported in part by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (No. 24580399).

References (22)

  • C.S. Hudak et al.

    Pref-1, a gatekeeper of adipogenesis

    Front. Endocrinol.

    (2013)
  • Cited by (10)

    • Effect of the anatomical site on telomere length and pref-1 gene expression in bovine adipose tissues

      2015, Biochemical and Biophysical Research Communications
      Citation Excerpt :

      The telomere to single copy gene ratio (T/S ratio) was calculated as an indicator of telomere length. Adipocyte size was measured as described previously [13,17]. In brief, the adipose tissue samples were fixed with 50 mM of collidine-HCl buffer (pH 7.4) containing 2% osmium tetroxide.

    • Localization and abundance of early markers of fat cell differentiation in the skeletal muscle of cattle during growth - Are DLK1-positive cells the origin of marbling flecks?

      2015, Meat Science
      Citation Excerpt :

      Together with higher CEBPB abundance in JB, this might have contributed to the development of more adipocytes in the skeletal muscle of JB. Comparable results for DLK1 mRNA expression in SCF of JB (Wagyu) and HS were reported by Yamada, Higuchi, and Nakanishi (2014). A relatively low expression of DLK1 in subcutaneous compared with mesenteric adipose tissue was associated with higher differentiation capability of subcutaneous adipocytes in vitro as reported by Tchkonia et al. (2002).

    View all citing articles on Scopus
    View full text