Variations in Tissue-Specific Expression of Adipose Differentiation-Related Protein Gene in Two Native Yunnan Chicken Breeds

B Zhang D Xiang R Yang L Yang J Li Z Zhao About the authors

ABSTRACT

Adipose differentiation-related protein (ADFP) is a fatty acid-binding protein that can promote the absorption of long-chain fatty acids. However, few results have been published regarding its role in Yunnan Native chicken breeds. The aim of this study was to determine ADFP gene tissue-specific expression in Piao chickens (PC) and Wuliangshan black-bone chickens (WBC) by RT-qPCR. The ontogenetic expression levels of the ADFP gene were significantly different during growth and development phases in the subcutaneous fat, liver, and pectoralis muscle of PC, and in the subcutaneous fat, liver, and pectoralis muscle of WBC (p<0.05). Individual tissue-differential expression levelswere detectedon d 91 and 112 in PC, with highest levels determined in abdominal fat and subcutaneous fat, respectively. However, in WBC, the highest levels were determined on d 49, 91 and 112 d in the pectoralis muscle and liver. Correlation analysis revealed ADFP expression level in liver of WBC was significantly related with LW and HC (p<0.05), while no significant correlations with carcass fatness (CF) were found in PC (p>0.05). The results suggest ADFPdifferential expression in the liver and pectoral muscles of PC and WBC during the growth and development phases (p<0.05). The observed expression patterns indicate that the ADFP gene plays an important role in lipid metabolism of PC and WBC, and that these patterns are expressed differently in the tissues of different chicken genotypes.

Keywords:
ADFP; carcass fatness; Piao chickens; RT-qPCR; Wuliangshan black-bone chickens

INTRODUCTION

Fat content and distribution in the carcass are not only economically-important traits in livestock, but also key factors affecting meat color, tenderness, taste, and other meat quality traits (Chen et al., 2008Chen JL, Zhao GP, Zheng MQ, Wen J, Yang N. Estimation of genetic parameters for contents of intramuscular fat and inosine-5'-monophosphate and carcass traits in chinese Beijing-you chickens. Poultry Science 2008;87(6):1098-104.; Mossab et al., 2002Mossab A, Lessire M, Guillaumin S, Kouba M, Mourot J, Peiniau P, et al. Effect of dietary fats on hepatic lipid metabolism in the growing turkey. Comparative Biochemistry & Physiology Part B Biochemistry & Molecular Biology 2002;132(2):473-483.). Therefore, it is widely accepted that carcass fatness (CF) is one of the most important carcass traits that determine the meat quality of chickens (Jiang et al., 2000Jiang X, Groen AF. Chicken breeding with local breeds in China - a review. Asian Australasian Journal of Animal Sciences 2000;13(10):1482-1498.). According to Castellini et al. (2002Castellini C, Mugnai C, Dal BA. Effect of organic production system on broiler carcass and meat quality. Meat Science 2002;60(3):219-225.), intramuscular fat (IMF) content influences meat tenderness and taste. Carcasses with appropriate fat content may obtain higher chicken broiler market prices. On the other hand, because fat deposition per unit requires three times more energy than lean meat accretion per unit, excessive fat deposition reduces feed utilization (Boekholt et al., 1994Boekholt HA, Van GP, Schreurs VV, Los MJ, Leffering CP. Effect of dietary energy restriction on retention of protein, fat and energy in broiler chickens. British Poultry Science 1994;35(4):603-614.). In addition, obesity is also associated with fatty-liver syndrome, increased mortality, and reduced egg production and fertility in laying chickens (Lee et al., 1975Lee K, Flegal CJ, Wolford JH. Factors affecting liver fat accumulation and liver hemorrhages associated with fatty liver-hemorrhagic syndrome in laying chickens. Poultry Science 1975;54(2):374.). Consequently, it is important to study the genetic mechanism of fat synthesis and regulation in chickens.

Adipose differentiation-related protein (ADFP) is a fatty acid-binding protein that belongs to the perilipin-adipophilin-TIP47 protein family (Magra et al., 2006Magra AL, Mertz PS, Torday JS, Londos C. Role of adipose differentiation-related protein in lung surfactant production: a reassessment. Journal of Lipid Research 2006;47(11):2367.) and can promote the absorption of long-chain fatty acids (Tobin et al., 2006Tobin KA, Harsem NK, Dalen KT, Staff AC, Nebb HI, Duttaroy AK. Regulation of ADRP expression by long-chain polyunsaturated fatty acids in BeWo cells, a human placental choriocarcinoma cell line. Journal of Lipid Research 2006;47(4):815-823.). The mRNA sequence of ADFP was isolated for the first time from the cDNA library of mouse adipocytes by differential hybridization screening technique and it is shown to be expressed in almost all types of mammalian cells (Jiang & Serrero, 1992; Buechler et al., 2001Buechler C, Ritter M, Duong CQ, Orso E, Kapinsky M, Schmitz G. Adipophilin is a sensitive marker for lipid loading in human blood monocytes. Biochimica Biophysica Acta 2001;532(1/2):97-104.). It is reported that ADFP plays an important role in the process of lipid aggregation and nucleation to form new lipid droplets (Wang et al., 2003Wang SM, Hwang RD, Greenberg AS, Yeo HL. Temporal and spatial assembly of lipid droplet-associated proteins in 3T3-L1 preadipocytes. Histochemistry and Cell Biology 2003;120(4):285-292.). Chang et al. (2006Chang HJ, Li L, Paul A, Taniguchi S, Nannegari V, Heird WC, Chan L. Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Molecular and Cellular Biology 2006;26(3):1063.) observed that the developmental expression of ADFP mRNA in mouse lung tissue was accompanied by the deposition of triglycerides in the lung tissue, and that triglyceride storage in the liver was reduced by 60% after the ADFP gene was inactivated. These results indicate that the ADFP gene is an important marker of lipid deposition in the adipocytes, and may be used as a potential candidate gene influencing fat deposition in livestock.

Although many research studies have been devoted to the regulation of the ADFP gene in mammals, to the best of our knowledge, no studies on the role of the ADFP gene in Yunnan Native chicken breeds have been published, except for the research of Decai et al. (2017Decai X, Zhiyong Z, Bin Z, Zhongcheng H, Quanshu W, Jing L. correlation analysis of relative expression of apob, adfp and fatp1 with lipid metabolism in daweishan mini chickens. Brazilian Journal of Poultry Science 2017;19(1):151-158.). The objective of the present study was to detect the tissue-specific expression of the ADFP gene in Piao chickens (PC) and Wuliangshan black-bone chickens (WBC) in order elucidate its role in fat deposition in two Yunnan native chicken breeds.

MATERIALS AND METHODS

Experimental birds and sample collection

All experimental procedures were reviewed and approved by the Yunnan Animal Science and Veterinary Institute Ethics Committee.

Piao chickens (PC) and Wuliangshan black-bone chickens (WBC) are native breeds of the Yunnan province, China. Piao chickens are tailless and have muscular thighs, and are known for having low bone and high meat content, in addition of sweet and tender meat. Wuliangshan black-bone chickens have the “one green and three black” characteristics (green ear, and black skin, meat and bones) and are known for their tolerance to roughage, fast growth rate, high medicinal value and delicious meat. They are reared for meat and egg production.

Chickens were obtained from a farm located in Pu’er city, Yunnan Province, China. All birds had access to water and feed ad libitum. Feed was formulated to supply the National Research Council (NRC) requirements for broilers (Nick & Dale, 1994Nick D. National research council nutrient requirements of poultry. The Journal of Applied Poultry Research 1994;3(1):101-101.).

On five different days of the grow-out period, at days 28, 49, 70, 91, and 112 days of age, 12 individuals of each breed (six males and six females) were slaughtered, and the pectoralis muscle, liver, abdominal fat and subcutaneous fat were collected according to the sampling method of Decai et al. (2017Decai X, Zhiyong Z, Bin Z, Zhongcheng H, Quanshu W, Jing L. correlation analysis of relative expression of apob, adfp and fatp1 with lipid metabolism in daweishan mini chickens. Brazilian Journal of Poultry Science 2017;19(1):151-158.) and stored in liquid nitrogen at 80ºC. Live weight (LW), backfat thickness (BFT) (on the back midline and anterior to the uropygial gland) and comb weight (CW) were determined (Table 1).

Table 1
Partial fatness trait (CF) indicators of two Yunnan Native chicken breeds.

Total RNA extraction and cDNA synthesis

Total RNA was directly extracted from above tissues according to the manufacturer’s instructions using TRIZOL Reagent kit (Tian’gen, Beijing, China) and its concentration (400 ng/µL) and purity (OD260/ OD280=1.8 ~ 2.0) were detected using the Ultra Micro Nucleic Acid Protein Analyzer (AJ, Germany). Then, first strand of cDNA was synthesized using the protocol specified by the FastQuant cDNA first strand synthesis kit (Tian’gen, Beijing, China) and was subsequently used for quantitative real-time polymerase-chain reaction PCR (RT-qPCR) analysis.

Primer design

In this study, for the evaluation of relative ADFP gene expression, the b-actin gene was used as internal control. The primers used for ADFP mRNA (GenBank accession: NM_001031420.1) and b-actinmRNA (GenBank accession: NM_205518.1) amplification sequences are reported elsewhere (Decai et al., 2017Decai X, Zhiyong Z, Bin Z, Zhongcheng H, Quanshu W, Jing L. correlation analysis of relative expression of apob, adfp and fatp1 with lipid metabolism in daweishan mini chickens. Brazilian Journal of Poultry Science 2017;19(1):151-158.). All primer sequences were synthesized by Sangon Biotech Co., Ltd. (Shanghai, China)

Real-time quantitative PCR (RT-qPCR) system and conditions

The optimal reaction system and conditions were determined by experimentation. The SuperRealPreMix Plus kit (Tian’gen, Beijing, China) was used to prepare the qPCR reaction system (20 µL) according to the manufacturer’s instructions, including 2 x 10 µL SuperRealPreMix Plus, 0.6 µL (10 µmol/L) of forward and reverse primers, respectively, 1 µL (about 100 ng) cDNA, 50 x D 0.4 µL ROX Reference Dye, and 7.4 µL ddH2O. Each sample was tested in duplicate at least thrice. Then, the qPCR reaction system was performed in a Real-Time PCR System (Applied Biosystems 7500, Thermo Fisher Scientific, Germany) with the following program: 1 cycle at 95ºC for 30 s, followed by 40 cycles at 95ºC for 3 s, 60ºC for 30 s, and at 72ºC for 20 s. The melting curve was built according to the default condition of the system.

Statistical analysis

The relative expression levels of ADFP gene in the above tissues of chickens were calculated using the 2-DDCt method (Livak et al., 2001Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25(4):402-408.). And the data were presented as means ± SD. Ontogenetic expression and tissue-differential expression of the ADFP gene were analyzed with Duncan’s test of SPSS 18 software in two Yunnan Native chicken breeds. Correlation analysis between ADFP mRNA expression levels and CF were calculated using the Pearson method according to Decai et al. (2017Decai X, Zhiyong Z, Bin Z, Zhongcheng H, Quanshu W, Jing L. correlation analysis of relative expression of apob, adfp and fatp1 with lipid metabolism in daweishan mini chickens. Brazilian Journal of Poultry Science 2017;19(1):151-158.). P-values lower than 0.05 were considered significant.

RESULTS

Amplification plots and melting curves of the ADFP gene and internal control gene

The total RNA concentration and the OD260/OD280 values of all samples tested were approximately 400ng/µL and 1.8-2.0, respectively, which were available for the subsequent experimental. In addition, the results show that the efficiency and individual repeatability of the amplification plots (Figure 1) of all genes were very good. No primer dimer or nonspecific peaks were found in any genes according to the melting curves (Figure 2), showing that the amplified products were the specific products needed for this study, and the Ct values generated were reliable and could be used for statistical analysis.

Figure 1
Amplification plots of the ADFP and β-actin genes.

Figure 2
Melting curves of the ADFP and β-actin genes.

ADFP temporal expression during chicken development

We used the Ct value obtained on d 28 in each tissue as the control to compute the ADFP ontogenetic expression levelin PC and WBC at different points.

In PC birds, the ADFP expression level in subcutaneous fat was higher on d 70 d than on d 28, 49, and 112 (p<0.05); not significantly different (p>0.05) in abdominal fat among each growth points; higher in liver on d 70 and 91 compared with d 28, 49, and 112 (p<0.05); and higher in the pectoralis muscle on d 70 than on d 28 and 49 (p<0.05) (Figure 3A). Therefore, in PC birds, ADFP expression levels in the subcutaneous fat, liver, and pectoralis muscle were higher on d 70 and then declined on d 112.

Figure 3
ADFP temporal expression during chicken development phase. At each time point, Ct value was used as the control to compare ADFP expression level differences in different tissues of PC and WBC. Lower case letters indicate statistical significance (p<0.05). PC: Piao chickens, WBC: Wuliangshan black-bone chickens,SF: subcutaneous fat, AF: abdominal fat, L: liver, PM: pectoralis muscle.

In WBC birds, ADFP expression peaked on d 91, 112d, and 28 in the abdominal fat, liver, and pectoralis muscle, respectively (Figure 3B). ADFP expression levels in SF were not significantly different among growth points (p>0.05), but were significantly higher (p<0.05) in the abdominal fat on d 70, 91, and 112 compared with d 28, in the liver on d 112 compared with d 28, 49, 70, and 91, and in pectoralis muscle on d 28 compared with d 49, 70, and 112 (p<0.05).

ADFP temporal expression in different chicken tissues

Figure 4 summarizes the ADFP tissue-differential expression among several tissues in PC and WBC. At each time point, the Ct value of subcutaneous fat was used as the control to compare the ADFP expression level differences in different tissues of PC and WBC.

Figure 4
ADFP temporal expression in different chicken tissues. At each time point, SF Ct value was used as the control to compare ADFP expression level differencesin different tissues of PC and WBC. Lower case letters indicate statistical significance (p<0.05). PC: Piao chickens, WBC: Wuliangshan black-bone chickens,SF: subcutaneous fat, AF: abdominal fat, L: liver, PM: pectoralis muscle.

In PC, ADFP expression levels were higher in abdominal fat than that in subcutaneous fat and liver on d 91 (p<0.05), whereas on d 112, higher levels were determined in subcutaneous fat than that in abdominal fat and liver (p<0.05). No significant differences in ADFP expression levels were detected among tissues on d 28, 49, or 70 (p>0.05) (Figure 4A).

In WBC, higher ADFP expression level was determined in the pectoralis muscle compared with subcutaneous fat on d 49 (p<0.05), as well as in the liver compared with subcutaneous fat on d 91 and 112 (p<0.05). No significant ADFP expression level differences among tissues were determined on d 28 and 70 (p>0.05) (Figure 4B). The results showed that the ADFP tissue-differential expression was not observed until d 91 in PC, while it was observed already on d 49 in WBC.

Correlation analysis between ADFP gene with CF

The results of the correlation analysis of ADFP gene expression in different tissues with CF in PC and WBC are shown in Table 2. Although there was a weak correlation between the ADFP gene expression level in different tissues and CF in PC (|R|>0), there was no significant difference between them (p>0.05). However, significant positive correlations of ADFP gene expression level in the liver with LW and HC were obtained in WBC (p<0.05). ADFP gene expression level in the liver was negatively correlated with CF in PC, and positively correlated with CF in WBC. The correlation between the ADFP gene expression level in pectoralis muscle and CF in PC was opposite to that found in WBC.

Table 2
Correlation coefficients of the ADFP gene expression in different tissues with carcass fatness (CF) in PC and WBC.

Tissue-differential expression of the ADFP gene between PC and WBC

In order to clarify the roles of the ADFP gene in fat development, we further analyzed its tissue-differential expression between PC and WBC. In each tissue, the Ct values determined on d 28 in PC were used as controls to compare the ADFP tissue-differential expressionat different time points between PC and WBC. The results showed that the ADFP gene expression levels in the subcutaneous fat and abdominal fat were no significantly different at each time point between PC and WBC (p<0.05) (Figure 5). However, lower liver levels were obtained in PC than in WBC on d 28, 49, and 112 (p<0.05), but higher in PC on d 70 (p<0.05). In addition, lower ADFP gene expression levels were measured in the pectoralis muscle of PC compared with WBC on d 28 and 91 (p<0.05).

Figure 5
ADFP gene tissue-differential expression between PC and WBC. In each tissue, the Ct value on d 28 in PC was used as the control to compare the ADFP tissue-differential expression at different time points between PC and WBC. Lower case letters indicate statistical significance (p<0.05). PC: Piao chickens, WBC:Wuliangshan black-bone chickens,SF: subcutaneous fat, AF: abdominal fat, L: liver, PM: pectoralis muscle.

DISCUSSION

Several studies have shown that ADFP is involved in the lipid metabolism of macrophages (Larigauderie et al., 2006Larigauderie G, Cuaz-Pérolin C, Younes AB, Furman C, Lasselin C, Copin C, et al. Adipophilin increases triglyceride storage in human macrophages by stimulation of biosynthesis and inhibition of beta-oxidation. Febs Journal 2006;273(15):3498-3510.), stimulating lipid accumulation and lipid droplet formation in fibroblasts (Imamura et al., 2002Imamura M, Inoguchi T, Ikuyama S, Taniguchi S, Kobayashi K, Nakashima N, et al. ADRP stimulates lipid accumulation and lipid droplet formation in murine fibroblast. American Journal of Physiology-Endocrinology and Metabolism 2002;283(4):E775-83.), transfer of lipids between lipofibroblasts and EPII cells, and maintenance of triglyceride reserves (Chang et al., 2006Chang HJ, Li L, Paul A, Taniguchi S, Nannegari V, Heird WC, Chan L. Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Molecular and Cellular Biology 2006;26(3):1063.; Schultz et al., 2002Schultz CJ, Torres E, Londos C, Torday JS. Role of adipocyte differentiation-related protein in surfactant phospholipid synthesis by type II cells. American Journal of Physiology-Lung Cellular and Molecular Physiology 2002;283(2):L288.) through physiological processes. Further, previous studies found that the ADFP gene was associated not only with the production traits of dairy goats (Li et al., 2014Li ZJ, Guo WJ, Tian YD, Han RL, Sun YJ, Xue J, et al. Characterisation of the genetic effects of the ADFP gene and its association with production traits in dairy goats. Gene 2014;538(2):244-250.), but also with carotid atherosclerosis (Nuotio et al., 2007Nuotio K, Isoviita PM, Saksi J, Ijäs P, Pitkäniemi J, Sonninen R, et al. Adipophilin expression is increased in symptomatic carotid atherosclerosis: correlation with red blood cells and cholesterol crystals. Stroke 2007;38(6):1791-1798.), colorectal cancer (Matsubara et al., 2011Matsubara J, Honda K, Ono M, Sekine S, Tanaka Y, Kobayashi M, et al. Identification of adipophilin as a potential plasma biomarker for colorectal cancer using label-free quantitative mass spectrometry and protein microarray. Cancer Epidemiology Biomarkers & Prevention 2011;20(10):2195-2203.) and other prevalent human diseases. The reason may be that ADFP, as a phospholipid protein covered by lipid droplets, may promote the absorption and storage of fatty acids and regulate the synthesis and decomposition of lipids (Imamura et al., 2002; Robenek et al., 2006Robenek H, Hofnagel O, Buers I, Robenek MJ, Troyer D, Severs NJ. Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis. Journal of Cell Science 2006;119(20):4215-4224.). Consequently, these findings suggest that the ADFP gene may influence fat deposition in livestock.

The results of the present study showed that the ADFP gene is expressed in the abdominal fat, subcutaneous fat, liver and pectoralis muscle of both PC and WBC, which is consistent with previous research (Decai et al., 2017Decai X, Zhiyong Z, Bin Z, Zhongcheng H, Quanshu W, Jing L. correlation analysis of relative expression of apob, adfp and fatp1 with lipid metabolism in daweishan mini chickens. Brazilian Journal of Poultry Science 2017;19(1):151-158.; Brasaemle et al., 1997Brasaemle DL, Barber T, Wolins NE, Serrero G, Blanchette-Mackie EJ, Londos C. Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. Journal of Lipid Research 1997;38(11):2249-2263.; Zhao et al., 2010Zhao X, Zhu Q, Wang Y, Yang Z, Liu Y. Tissue-specific expression of the chicken adipose differen-tiation-related protein (ADP) gene. Molecular Biology Reports 2010;37(6):2839-2845.). In addition, ADFP gene expression level peaked in PC on d 70 in the liver, subcutaneous fat and pectoralis muscle, whereas in WBC, the highest ADFP expression levels in abdominal fat, liver, and pectoralis muscle were determined on d 91, 112, and 28, respectively. These results show that, compared with Sichuan Mountainous Black-bone chicken (Zhao et al., 2010) and Daweishan Mini chicken (Decai et al., 2017), liver lipid synthesis, fatty-acid absorption and storage in the subcutaneous fat and the pectoralis muscle of PC were relatively faster, with peak on d 70, whereas in WBC, peaks were observed on d 112, 91, and 28 in the liver, abdominal fat, and pectoralis muscle, respectively. This indicates that PC are most likely to gain fat at 10 weeks of age, while WBC are more likely to gain fat at 4, 13 and 16 weeks of age, respectively.

Previous studies reported that ADFP gene is expressed in muscle, lung, liver, kidney, brain and other tissues of adult rats, with highest expression in the tissue with the most neutral lipid (Yan et al., 2006Yan J, Burman A, Nichols C, Alila L, Showe L C, Showe M K, et al. Detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels with mouse microarrays. Physiological Genomics 2006;25(2):346-353.). In the present study, ADFP gene expression level of PC in the abdominal fat on d 91 was higher than that in the liver and subcutaneous fat (p<0.05), and higher in the subcutaneous fat on d 112 than that in the abdominal fat and liver (p<0.05). However, in WBC, higher ADFP gene expression level was found in the pectoralis muscle compared with subcutaneous fat on 49 d (p<0.05), and in the liver compared with subcutaneous fat on d 91 and 112 (p<0.05). These results suggest that, in PC, on d 91 and 112 d, lipids were mainly absorbed and stored in abdominal fat and subcutaneous fat, respectively, which was may be one of the reasons why PC has more tasty meat after 112 d. However, the ADFP gene expression in adipocytes of WBC was the same as that in Daweishan Mini chicken, i.e., its level in pectoralis muscle was, in general, higher than that in adipose tissue during the period of fast muscle growth (d 49 to 70) (Decai et al., 2017Decai X, Zhiyong Z, Bin Z, Zhongcheng H, Quanshu W, Jing L. correlation analysis of relative expression of apob, adfp and fatp1 with lipid metabolism in daweishan mini chickens. Brazilian Journal of Poultry Science 2017;19(1):151-158.). In addition, lipid synthesis in WBC between d 91 and 112 occurred in the liver, which is the main tissue of poultry triglyceride synthesis (Hermier, 1997Hermier D. Lipoprotein metabolism and fattening in poultry. Journal of Nutrition 1997;127(5 Suppl):805S.).

The correlation analysis showed that ADFP gene expression levels in different tissues of PC birds were not significantly correlated with CF, while its level in liver of WBC was significantly related to LW and HC. Further analysis showed ADFP gene expression in the liver and pectoral muscles of PC and WBC birds were different during the growth and development process, demonstrating the tissue-differential expression of the ADFP gene between PC and WBC.

ACKNOWLEDGMENTS

The assistance of the staff at Piao chickens farm and Wuliangshan black-bone chickens farm of Pu’er city is highly appreciated. The work was supported by the project for breeding and disseminating of Yunling quality broilers. This work was funded by grants provided by the National Natural Science Foundation of China (31200924), the Applied Basic Research programs of Yunnan Province (2010ZC162) and by the Scientific Research Foundation of Kunming University (YJL11003).

REFERENCES

  • Boekholt HA, Van GP, Schreurs VV, Los MJ, Leffering CP. Effect of dietary energy restriction on retention of protein, fat and energy in broiler chickens. British Poultry Science 1994;35(4):603-614.
  • Nick D. National research council nutrient requirements of poultry. The Journal of Applied Poultry Research 1994;3(1):101-101.
  • Brasaemle DL, Barber T, Wolins NE, Serrero G, Blanchette-Mackie EJ, Londos C. Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. Journal of Lipid Research 1997;38(11):2249-2263.
  • Buechler C, Ritter M, Duong CQ, Orso E, Kapinsky M, Schmitz G. Adipophilin is a sensitive marker for lipid loading in human blood monocytes. Biochimica Biophysica Acta 2001;532(1/2):97-104.
  • Castellini C, Mugnai C, Dal BA. Effect of organic production system on broiler carcass and meat quality. Meat Science 2002;60(3):219-225.
  • Chang HJ, Li L, Paul A, Taniguchi S, Nannegari V, Heird WC, Chan L. Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Molecular and Cellular Biology 2006;26(3):1063.
  • Chen JL, Zhao GP, Zheng MQ, Wen J, Yang N. Estimation of genetic parameters for contents of intramuscular fat and inosine-5'-monophosphate and carcass traits in chinese Beijing-you chickens. Poultry Science 2008;87(6):1098-104.
  • Decai X, Zhiyong Z, Bin Z, Zhongcheng H, Quanshu W, Jing L. correlation analysis of relative expression of apob, adfp and fatp1 with lipid metabolism in daweishan mini chickens. Brazilian Journal of Poultry Science 2017;19(1):151-158.
  • Hermier D. Lipoprotein metabolism and fattening in poultry. Journal of Nutrition 1997;127(5 Suppl):805S.
  • Imamura M, Inoguchi T, Ikuyama S, Taniguchi S, Kobayashi K, Nakashima N, et al. ADRP stimulates lipid accumulation and lipid droplet formation in murine fibroblast. American Journal of Physiology-Endocrinology and Metabolism 2002;283(4):E775-83.
  • Jiang H P, Serrero G. Isolation and characterization of a full-length cDNA coding for an adipose differentiation-related protein. Proceedings of the National Academy of Sciences of the United States of America 1992;89(17):7856-60.
  • Jiang X, Groen AF. Chicken breeding with local breeds in China - a review. Asian Australasian Journal of Animal Sciences 2000;13(10):1482-1498.
  • Larigauderie G, Cuaz-Pérolin C, Younes AB, Furman C, Lasselin C, Copin C, et al. Adipophilin increases triglyceride storage in human macrophages by stimulation of biosynthesis and inhibition of beta-oxidation. Febs Journal 2006;273(15):3498-3510.
  • Lee K, Flegal CJ, Wolford JH. Factors affecting liver fat accumulation and liver hemorrhages associated with fatty liver-hemorrhagic syndrome in laying chickens. Poultry Science 1975;54(2):374.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25(4):402-408.
  • Li ZJ, Guo WJ, Tian YD, Han RL, Sun YJ, Xue J, et al. Characterisation of the genetic effects of the ADFP gene and its association with production traits in dairy goats. Gene 2014;538(2):244-250.
  • Magra AL, Mertz PS, Torday JS, Londos C. Role of adipose differentiation-related protein in lung surfactant production: a reassessment. Journal of Lipid Research 2006;47(11):2367.
  • Matsubara J, Honda K, Ono M, Sekine S, Tanaka Y, Kobayashi M, et al. Identification of adipophilin as a potential plasma biomarker for colorectal cancer using label-free quantitative mass spectrometry and protein microarray. Cancer Epidemiology Biomarkers & Prevention 2011;20(10):2195-2203.
  • Mossab A, Lessire M, Guillaumin S, Kouba M, Mourot J, Peiniau P, et al. Effect of dietary fats on hepatic lipid metabolism in the growing turkey. Comparative Biochemistry & Physiology Part B Biochemistry & Molecular Biology 2002;132(2):473-483.
  • Nuotio K, Isoviita PM, Saksi J, Ijäs P, Pitkäniemi J, Sonninen R, et al. Adipophilin expression is increased in symptomatic carotid atherosclerosis: correlation with red blood cells and cholesterol crystals. Stroke 2007;38(6):1791-1798.
  • Robenek H, Hofnagel O, Buers I, Robenek MJ, Troyer D, Severs NJ. Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis. Journal of Cell Science 2006;119(20):4215-4224.
  • Schultz CJ, Torres E, Londos C, Torday JS. Role of adipocyte differentiation-related protein in surfactant phospholipid synthesis by type II cells. American Journal of Physiology-Lung Cellular and Molecular Physiology 2002;283(2):L288.
  • Tobin KA, Harsem NK, Dalen KT, Staff AC, Nebb HI, Duttaroy AK. Regulation of ADRP expression by long-chain polyunsaturated fatty acids in BeWo cells, a human placental choriocarcinoma cell line. Journal of Lipid Research 2006;47(4):815-823.
  • Wang SM, Hwang RD, Greenberg AS, Yeo HL. Temporal and spatial assembly of lipid droplet-associated proteins in 3T3-L1 preadipocytes. Histochemistry and Cell Biology 2003;120(4):285-292.
  • Yan J, Burman A, Nichols C, Alila L, Showe L C, Showe M K, et al. Detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels with mouse microarrays. Physiological Genomics 2006;25(2):346-353.
  • Zhao X, Zhu Q, Wang Y, Yang Z, Liu Y. Tissue-specific expression of the chicken adipose differen-tiation-related protein (ADP) gene. Molecular Biology Reports 2010;37(6):2839-2845.

Publication Dates

  • Publication in this collection
    09 May 2019
  • Date of issue
    Jan-Mar 2019

History

  • Received
    19 Mar 2018
  • Accepted
    10 Aug 2018
Fundação APINCO de Ciência e Tecnologia Avícolas Av. Andrade Neves, 2501 - Castelo, 13070-001 Campinas SP - Brazil, Tel.: (55 19) 3243-6555 / Fax.: (55 19) 3243-8542 - Campinas - SP - Brazil
E-mail: rvfacta@terra.com.br