Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (13): 2674-2686.doi: 10.3864/j.issn.0578-1752.2024.13.014

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

Cloning, Expression Characterization, and Functional Analysis of the Snail1 in Qinchuan Cattle and Its Impact on Proliferation of Bovine Adipocytes

ZHU BingLin1(), YU JiaLi1, CHEN JiaYue1, TIAN Yuan1, WAN Yuan1, LIU ChenYang1, WANG XiaoYu1, WANG MiaoLi1, CHENG Gong1,2()   

  1. 1 College of Animal Science and Technology, Northwest A&F University, Yangling 712100, Shaanxi
    2 National Beef Cattle Improvement Center, Yangling 712100, Shaanxi
  • Received:2023-12-23 Accepted:2024-05-14 Online:2024-07-09 Published:2024-07-09
  • Contact: CHENG Gong

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Abstract:

【Objective】 The deposition of intramuscular fat in beef cattle is closely associated with the flavor, juiciness, and tenderness of beef, characterized by the proliferation (increased in number) and differentiation (lipid deposition) of fat cells, which is regulated by multiple genes. The previous studies have indicated that Snail1 is involved in muscle development and lipid homeostasis in mice; however, its role in bovine adipogenesis remains unknown, which warrants further investigation. 【Method】 Snail1 gene CDS region sequence was cloned from Qinchuan cattle, Snail1 gene temporal and spatial expression profile was constructed, and its functional structure and target gene were predicted by bioinformatics software. Subsequently, the impact of Snail1 on the proliferation of bovine adipocytes was explored through RNAi interference, along with CCK8, EdU, cell flow cytometry, and RT-qPCR methods. 【Result】 Compared with the sequence published by NCBI, the Snail1 gene in Qinchuan cattle had two synonymous mutations. The Snail1 gene exhibited higher abundance expression in newborn cattle lung, perirenal fat, and small intestine. However, in the adult cattle, the expression level of the Snail1 gene was the highest in perirenal fat tissue, followed by longissimus dorsi muscle, and lowest in lung tissue. Bioinformatics analysis revealed a 651 bp CpG island in the Snail1 promoter region, along with binding sites for transcription factors related to fat formation, such as C/EBP and PPARα. CKⅠ (Ser92/96), CKⅡ (Ser25/119, Thr89), CDK1 (Ser13/104/112/119/143/221/183/214), CDK5 (Ser105/107), and other cell cycle related kinases could participate in the Snail1 phosphorylation of proteins. By extracting promoter regions of bovine annotated genes, predicting target genes and constructing KEGG dynamic networks, it was found that lipid formation related signaling pathways, such as MAPK, PI3K-Akt and mTOR, were potential node signaling pathways involving in Snail1’s involvement in adipogenesis. Further functional studies through RNAi interference demonstrated that downregulation of the Snail1 gene promoted the proliferation of bovine preadipocytes, increased the proportion of cells in the S phase (P<0.01), and facilitated G1/S cell cycle transition. RT-qPCR and Western blot analysis indicated that interfering with the Snail1 gene significantly upregulated the expression of proliferation- regulating genes, including CCNB1, CCND2, CDK2, and CDK4 (P<0.05), at both the genes and protein levels. 【Conclusion】 The expression of Snail1 gene was relatively high in neonatal and adult perirenal fat and longissimus dorsi muscle. Interfering with the Snail1 gene promoted the proliferation of bovine preadipocytes and the G1/S cell cycle transition, as well as the expression of CCNB1, CCND2, CDK2, CDK4, and other proliferation-related genes. Cell cycle-related kinases, including CKⅠ, CKⅡ, and CDK1/5, could participate in the regulation of cell proliferation through the phosphorylation modification of Snail1 protein. Furthermore, the MAPK, PI3K-Akt, and mTOR pathways were potential node signaling pathways influenced by Snail1. This study established a foundation for further exploration of the mechanism by which Snail1 participated in bovine fat formation.

Key words: cattle, Snail1, fat deposition, KEGG dynamic network, RNAi, cell proliferation

Table 1

Primer information"

引物
Primer		 引物序列
Primer sequences (5′-3′）		 退火温度
Annealing temperature (℃)		 产物长度
Product length (bp)		 用途
Application
Snail1-cds F: GCGGGTGGAGGGTTTTGC
R: ACGAGGGGATTCTGTGGC		 55 977 编码区克隆
Coding region cloning
Snail1 F：GCACGACTCTTCTCCAGA
R: AGATGAGTGTCGGCAAGG		 60 116 实时荧光定量PCR
Real-time qPCR
CCNB1 F：TGATGGAACTAACTATGCTGG
R：GCATAACAACGAGAAGGGATT		 165
CCND2 F：GGGCAAGTTGAAATGGAA
R：TCATCGACGGCGGGTAC		 173
CDK2 F：GGGTCCCTGTTCGTACTTATAC
R：CCACTGCTGTGGAGTAGTATTT		 96
CDK4 AGACCTCGAGTGTATGGCG
CCCTACAATCACAGAGGCTCAA		 110
CCNA2 F：GCAGCCTTTCATTTAGCACTCT
R：ATTGACTGTTGTGCGTGCTG		 155
MAP4K4 F：ACACGTAAGAAAGAACCCACACT
R：GCCAGTTTCCACAGATCGGA		 259
PHLPP1 F：ACGGAGTGGACTTTCTCCCT
R：TTTCGGCTTTCACAGACCCA		 280
PHLPP2 F:CCTTGGCTGTATGCTCCGAT
R:AAGATAGGTCTGCGCTTGGG		 292
MAPKAP1 F:AGCAGCCACCACTACAAGTC
R:TATTGCGTGACTGGGGCTTT		 222
GAPDH F:AGTTCAACGGCACAGTCAAGG
R: ACCACATACTCAGCACCAGCA		 124
β-actin F: TCTAGGCGGACTGTTAGC
R: CCATGCCAATCTCATCTCG		 82

Fig. 1

PCR amplification of Snail1 and sequence alignment M represents DL2000 DNA Marker; L1- L4 represents PCR amplification product of Snail1"

Fig. 2

Expression profile of Snail1 in new born and adult cattle A. Newborn cattle; B. Adult cattle"

Fig. 3

Prediction of Snail1 protein domain and secondary/tertiary structure A and B: Prediction results of secondary structure of Qinchuan cattle Snail1 protein; C: Prediction results of Snail1 protein domain in Qinchuan cattle; D: Prediction of the tertiary structure of Qinchuan cattle Snail1 protein"

Fig. 4

Prediction of CpG island in promoter region of bovine Snail1 and binding site of transcription factor"

Fig. 5

Distribution of phosphorylation sites of Snail1 protein"

Fig. 6

KEGG cluster analysis and dynamic network drawing of Snail1 target gene A. The top20 KEGG pathways enriched by putative targeting genes of Snail1; B. Dynamic network construction of adipogenesis related pathways"

Table 2

KEGG network diagram and potential target genes of Snail1 in related signaling pathways"

信号通路
Pathways		 互作值
Degree		 信号通路潜在靶基因
Potential target genes in the pathways
MAPK 信号通路 MAPK signaling pathway 9 PTP, MKP（MAP4K4）, HGK, JIP1/2 (MAPK8IP1/2), PP2CB, TAO, etc.
PI3K-Akt 信号通路 PI3K-Akt signaling pathway 8 PHLPP1/2, TCL1, etc.
mTOR 信号通路 mTOR signaling pathway 5 TBC1D7, MAPKAP1, RICTOR, FNIP, TTI1, CLIP1, etc.
癌症相关信号通路 Pathways in cancer 5 KNG1, ARHGEF12, PLEKHG5, etc.

Fig. 7

Detection of the impact of RNA interference of Snail1 on the expression of potential target genes"

Fig. 8

The impact on proliferation of bovine preadipocytes by Snail1 A: The impact on preadipocytes proliferation by RNA interference of Snail1 detected by CCK8; B：The RNA interference analysis; C: The impact on preadipocytes proliferation by RNA interference of Snail1 detected by EdU. The EdU positive cells showed Red (EdU), nuclear showed blue(DAPI); D: The quantity of EdU dying results; E: The impact on cell cycle by RNA interference of Snail1; F: The quantity of cell cycle results"

Fig. 9

The influence on proliferation maker genes of bovine preadipocytes by Snail1 A-E: The impact on the mRNA expression levels of proliferation-related genes CCNB1, CCND2, CDK2, CDK4, and CCNA2 by down regulation of Snail1; F: The protein level of CCNB1 and CCND2 detected by Western-blot"

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