Indian Journal of Animal Research

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Research Article

Indian Journal of Animal Research, volume 55 issue 5 (may 2021) : 536-541

The Differential Expressions of PPARγ and CAST mRNA in Muscle Tissues of Jinhua and Landrace Pigs

Weixin Zhao1, Liping Guo1, Zhiguo Miao1,*, Jinzhou Zhang1, Shan Wang1
1College of Animal Science and Veterinary Medicine, Henan Institute of Science and Technology, Xinxiang, Henan, 453003, P.R. China.
Cite article:- Zhao Weixin, Guo Liping, Miao Zhiguo, Zhang Jinzhou, Wang Shan (2020). The Differential Expressions of PPARγ and CAST mRNA in Muscle Tissues of Jinhua and Landrace Pigs . Indian Journal of Animal Research. 55(5): 536-541. doi: 10.18805/ijar.B-1272.

ABSTRACT

Background: Fat deposition affected meat quality and the suitable amount of intramuscular fat (IMF) can significantly improve the taste of meat, palatability, juicy, tenderness and flavor, thereby enhancing the meat quality in animals. Although, calpastatin (CAST) and peroxisome proliferator-activated receptor-γ (PPARγ) could regulate meat quality by altering meat tenderness or IMF content in animals, reports concerning the relationship between CAST, PPARã expression and pork quality is unclear.

Methods: A total of twenty 28-day-old purebred weaned Jinhua and Landrace piglets (10 piglets per breed) were divided into two groups according to breed for the feeding trials lasting for 120 days. At the 148 days of age, 3 pigs of each breed were selected to slaughter. Total RNA was extracted from longissimus dorsi and biceps femoris muscle to investigate the differential expression of PPARã and CAST in muscle tissues of different breed pigs by RT-PCR methods, as well as their relationship with IMF and carcass lean content.

Result: These results suggested that PPARã is an important effector for regulating fat deposition in pigs, which was correlated with IMF and carcass lean content of pigs. This data would provide a scientific basis for the regulation of pork quality.

INTRODUCTION

Meat quality is usually affected by many factors, such as genotypes, nutrition, age, composition, and distribution of carcass fat and so on (O’Quinn et al., 2012; Chen et al., 2016; Lee et al., 2017). Numerous studies have demonstrated that fat deposition affected meat quality and the suitable amount of intramuscular fat (IMF) can significantly improve the taste of meat, palatability, juicy, tenderness and flavor, thereby enhancing the meat quality in animals (Hunt et al., 2014; Bauer et al., 2016; Leal-Gutiérrez et al., 2018). IMF is distributed in skeletal muscle, and there is a positive correlation between IMF content and meat tenderness (Houbak et al., 2008; Magnabosco et al., 2016). It is well known that peroxisome proliferator-activated receptor gamma (PPARγ) is a member of the transcription factor nuclear receptor superfamily, which is a critical regulator of adipogenesis, glycolipid metabolism and cell proliferation and differentiation (Kersten et al., 2000; Wang et al., 2017). PPARγ is not only a regulator of adipose tissue development, but also modulates a variety of genes expression involved in fatty acid transport and metabolism at the transcriptional level (Freitag and Miller, 2014). Cui et al., (2016) observed that PPARγ mRNA expression was significantly and positively correlated with IMF deposition in Laiwu, Lulai Black, and Large White pigs. Ma et al., (2015) indicated that PPARγ enhanced the IMF content in pigs, and improved pork quality. These results suggested that PPARγ could improve meat quality by regulating IMF content in animals.
        
Meat tenderness is also one of the important traits of pork quality (Ouali et al., 2006). CAST is an endogenous calpain protein that requires Ca2+ activation, which inhibits the degradation of myofibrillar proteins and reduces the growth rate of myofibroblasts (Gandolfi et al., 2011). After slaughter of animals, CAST could affect meat tenderness through inhibiting protease activity and reducing protein hydrolysis which regulating meat quality (Huff-Lonergan and Lonergan, 2005). Calvo et al., (2014) found that meat tenderness in beef is affected by calpastatin (CAST) expression and there is a negative correlation between the CAST expression and meat tenderness. Li et al., (2013) observed that muscle tenderness in Yanbian cattle could be increased by activating calpain or reducing CAST activity, which altering meat quality.
        
The Jinhua pig, a famous local breed in China, is characterized by high IMF content, good tenderness and excellent meat quality (Guo et al., 2011). Whereas, Landrace has high lean meat content and lower tenderness (Velotto et al., 2014; Xiao et al., 2018). Therefore, these two breed pigs are ideal models for studying regulation and molecular mechanism of pork quality. Although, CAST and PPARγ could regulate meat quality by altering meat tenderness or IMF content in animals, reports concerning the differential expressions of CAST, PPARγ mRNA in muscle tissues of Jinhua and Landrace pigs, as well as about the relationship between CAST, PPARγ expression and pork quality in two breed pigs are unclear. Hence, Jinhua and landrace pigs with differential meat quality were used in this present study to investigate differential expressions of CAST and PPARγ mRNA in muscle tissues and their effects on the carcass composition, intramuscular fat and meat quality. This data will provide a scientific basis for the regulation of pork quality.

MATERIALS AND METHODS

Experimental design and animals
 
All pigs handing protocols in this study was approved by the Animal Care and use Committee of Henan Institute Science and Technology (Xinxiang, P.R. China). A total of twenty 28-day-old purebred weaned Jinhua and Landrace piglets (10 piglets per breed) were divided into two groups according to breed for the feeding trials lasting for 120 days. These experiments were done at Laboratory Animal Center, Henan Institute of Science and Technology, from March of 2019 to July of 2019. The experimental diets were formulated to meet National Research council (NRC, 1998) nutrient requirements for pigs. All pigs were reared in the same condition and had ad libitum access to an experimental diet and water via nipple drinkers. At the 148 days of age, 3 pigs of each breed were selected to slaughter according to the method described by Miao et al., (2009), longissimus dorsi and biceps femoris muscle tissues were quickly collected and frozen in liquid nitrogen and then stored at -80°C in a refrigerator until further analysis. Left half carcass without head, hoofs, tail and guts (contained kidney) were weighed and carcass lean tissue was dissected and weighed to calculate the carcass lean content. The analysis of IMF in longissimus dorsi and biceps femoris muscle was performed according to the AOAC (1990) procedures.
 
RNA extraction and cDNA synthesis
 
Total RNA of longissimus dorsi and biceps femoris muscle was extracted using TRIZOL reagent (Invitrogen, Carlsbad, CA, USA) and then removed DNA via DNase treatment (NEB, Ipswich, MA, USA). The RNA concentration and purity were tested using a Nanodrop spectrophotometer (Thermo-Scientific, Wilmington, DE) and the integrity of RNA was checked with 1% agarose gel. Approximately 1 μg of the total RNA in each sample was used to synthesize cDNA by PrimeScript™ RT Reagent Kit (Takara Bio Inc., Tokyo, Japan).
 
Primer design
 
Primers for amplifying PPARγ, CAST and β­actin mRNA were designed on the basis of known sequences deposited in GeneBank using Primer 5.0 software (Lalitha, 2000) and all primer sequences are shown in Table 1.
 

Table 1: Parameters of gene-specific primers for PPARã, CAST and ACTB genes.


 
Real-time quantitative PCR (qRT-PCR)
 
The relative expression of the target gene was determined by quantitative real-time PCR amplification using an iQ5 RT-PCR detection system (Bio-Rad Laboratories, Hercules, CA). Dissociation melt curve analyses were performed to verify the specificity of the PCR products. Relative expression levels of PPARγ, CAST mRNA were determined after normalization to β-actin reference using 2-ΔΔCT method.
 
Statistical analysis
 
The differential results between experimental groups were analyzed by student’s t-test and all data analyses were performed using SPSS 17.0 (SPSS, 2004) statistical software. Significant differences between Jinhua and Landrace groups were measured at P<0.05. Bivariate correlations were used to evaluate the correlation between carcass lean, IMF content and gene expression. The data are presented as means±SEM.

RESULTS AND DISCUSSION

Carcass lean and IMF content
 
The IMF of longissimus dorsi and biceps femoris muscle, and carcass lean content in Jinhua and Landrace pigs were shown in Fig 1(A) and Fig 1(B). Compared with Landrace pigs, Jinhua pigs had higher IMF content of longissimus dorsi and biceps femoris muscle (P<0.05). Whereas, carcass lean content of Jinhua pigs was lower than those of Landrace pigs (P<0.01).
 

Fig 1(A): The differences in IMF content of longissimus dorsi and biceps femoris muscle in Jinhua and Landrace pigs. 1(B): The differences in carcass lean content of Jinhua and Landrace pigs.


        
Pervious results have shown that many factors affected IMF and carcass lean content, such as genotypes, nutrition, age and so on (Insausti et al., 2005; Zhang and Guan, 2019). Carcass lean and IMF content is essential for eating quality, palatability, taste and flavor of meat (Huang et al., 2012). In this present study, Jinhua pigs had higher IMF and lower carcass lean content compared with Landrace, which suggested that IMF and carcass lean content was affected by different genetic types of pigs (Wanger et al., 1999). The results are in accordance with previous reports (Miao et al., 2009), who observed that Jinhua pig with higher IMF content had better meat quality compared with Landrace pigs. Similar results were reported during studies on Meishan, Iberian pigs, or Creole pigs when compared with lean meat type pigs (White et al., 1995; Morales et al., 2003; Renaudeau and Mourot, 2007). These results demonstrated that there are significant differences in carcass lean and IMF content between differential breed pigs.
 
PPARγ and CAST gene expression
 
PPARγ expression of longissimus dorsi and biceps femoris muscle in Jinhua and Landrace pigs was shown in Fig 2(A). Compared with Landrace pigs, Jinhua pigs had higher PPARγ mRNA expression concentration (P<0.01). Mean while, PPARγ mRNA expression of longissimus dorsi muscle was lower than that of biceps femoris muscle in two breed pigs (P<0.05). CAST mRNA expression of Jinhua and Landrace pigs was shown in Fig 2(B). The CAST mRNA expression in longissimus dorsi and biceps femoris muscle of Jinhua pigs were significantly higher than those of Landrace pigs (P<0.05). Whereas, there were no differences in CAST mRNA expression between longissimus dorsi and biceps femoris muscle of two breeds (P>0.05).
 

Fig 2(A): The differential expression of PPARã mRNA in muscle tissues of Jinhua and Landrace pigs. 2(B): The differential expression of CAST mRNA in muscle tissues of Jinhua and Landrace pigs.


 
PPARγ is a pivotal transcription factor, which regulating energy and lipid metabolism, lipogenesis process, as well as mammalian adipocyte differentiation and fat deposition (Chang and Cho, 2012; Zeng et al., 2012; He et al., 2013). Cui et al., (2016) also reported that PPARγ regulated genes expression concerning sugar metabolism and lipid biosynthesis. In this present study, there was a significant difference in PPARγ expression of longissimus dorsi and biceps femoris muscle between Jinhua and Landrace pigs, which suggested that IMF deposition was different between two breeds. These results are in accordance with previous finding of Cui et al., (2016) who observed that there was difference in PPARγ expression concentrations of longissimus dorsi muscle tissues among Laiwu, Lulai Black and Large White pigs. In addition, we also found that there were differences in the PPARγ expression between longissimus dorsi and biceps femoris muscle of the same breeds, which might be a reason for their different IMF content. Cui et al., (2016) also demonstrated that PPARγ gene is a vital effector of IMF content in longissimus dorsi muscle of pigs. These results indicated that PPARγ could be used as a candidate gene of pork quality (Ma et al., 2015).
        
Previous study showed that CAST regulates post-mortem proteolysis and affected the process of muscle tenderization (Kemp et al., 2010). Therefore, the CAST gene is a candidate gene for meat quality in livestock. The expression level of CAST mRNA was closely related to IMF content and affected meat tenderness in muscle tissues of pigs (Gandolfi et al., 2011; Ropka-Molik et al., 2014). Li et al., (2013) also observed that CAST gene was correlated with meat tenderness height and highly correlated with the fatty acid and the amino acid content, which is a potential marker for meat quality in Yanbian cattle. In this present study, the CAST expression in longissimus dorsi and biceps femoris muscle of Jinhua pigs was higher than that of Landrace pigs. These results suggested that Jinhua pigs had higher tenderness and better meat quality compared with Landrace pigs.
 
The relationship between gene expression and carcass lean, IMF content
 
As shown in Table 2, the relationship between PPARγ, CAST mRNA expression and carcass lean, IMF content was analyzed by bivariate correlations. The PPARγ mRNA expression in longissimus dorsi and biceps femoris muscle was positively correlated with IMF content in Jinhua pigs (PPARγ/IMF content: r=0.590, P =0.043, r=0.713, P=0.009, respectively). The similar results were found in Landrace pigs (PPARγ/IMF content: r=0.740, P=0.006, r=0.632, P=0.027, respectively). Whereas, the expression of PPARγ mRNA in two muscle tissues was negatively correlated with carcass lean content in Jinhua pigs (PPARγ/IMF content: r=-0.684, P=0.014, r=-0.738, P=0.006, respectively). The similar results were found in Landrace pigs (PPARγ/IMF content: r=-0.704, P=0.011, r=-0.650, P=0.022, respectively). In addition, the expression of CAST mRNA in the two muscle tissues had no severe relationship with IMF and carcass lean content of two breed pigs (P>0.05).
 

Table 2: The relationship between of PPARã, CAST mRNA expression and IMF, carcass lean content.


        
PPARγ is involved in the adipocyte differentiation and improved IMF deposition and adipogenesis in muscle fibers which determines IMF content (Wang et al., 2013). In the present experiment, the PPARγ expression in muscle tissues of Jinhua and Landrace pigs was significantly and positively correlated with IMF content. This result indicated that PPARγ is very important for fat accumulation in muscle tissues of pigs. Similar results are reported by Wang et al., (2013), who observed that the expression of PPARγ mRNA is positively correlated with IMF in the longissimus dorsi muscles of Erhualian pigs. Cui et al., (2016) also found that PPARγ mRNA expression was positively correlated with IMF deposition in longissimus dorsi muscle of Laiwu, Lulai Black and Large White pigs, which suggested that PPARγ gene was a main effector of IMF content. In addition, our research found that PPARγ expression was negatively correlated with carcass lean content in the two breeds of pigs. The results suggested that PPARγ might affect muscle growth and development to alter carcass lean content in pigs. However, the molecular mechanism between PPARγ expression and muscle development is unclear and need to be identified in further studies.
 
Previous research has showed that CAST have an important effect on tenderness. Meat quality and tenderness could be improved by activating calpain or reducing CAST activity (Colle et al., 2018). The CAST gene is an important marker for pork quality and carcass traits (Djurkin et al., 2016). In this study, the CAST expression in longissimus dorsi and biceps femoris muscle was not correlated with IMF and carcass lean content of the two breeds. These results indicated that the IMF and carcass lean content is not significantly affected by CAST gene expression. Wu et al., (2007) found that CAST was significantly correlated with diameter, area, circularity, and the aspect ratio of muscle fiber, but not with carcass lean and IMF content of pigs. Although the association between CAST mRNA expression and meat quality has been reported on cattle and pigs (Chung et al., 2001; Koćwin-Podsiadla et al., 2003), how CAST affects meat quality in other animals and its molecular mechanism need to be further studied.

CONCLUSION

PPARγ is an important effector for regulating fat deposition in pigs as PPARγ gene expression was correlated with IMF and carcass lean content of pigs. The data would provide new information to elucidate the molecular mechanism of IMF deposition in Jinhua pigs and Landrace pigs. In addition, this study also revealed that IMF and carcass lean content in pigs was not significantly affected by CAST gene expression.

ACKNOWLEDGEMENT

This study was supported by grants from the National Natural Science Foundation of China (31572417), the Henan joint funds of National Natural Science Foundation of China (U1604102) and Provincial key Technology Research and development program of Henan (192102110069).

CONFLICT OF INTEREST

We declare that we have no conflict of interest.

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