Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (6): 1191-1203.doi: 10.3864/j.issn.0578-1752.2024.06.013

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

Study on the Role of FoxO1 in Regulating the Proliferation, Apoptosis and Differentiation of Bovine Skeletal Muscle Cells

JIANG Chao1(), ZHANG JiuPan2, SONG YaPing1, SONG XiaoYu1, WU Hao1, WEI DaWei1()   

  1. 1 College of Animal Science and Technology, Ningxia University/Key Laboratory of Ruminant Molecular Cell Breeding, Ningxia Hui Autonomous Region, Yinchuan 750021
    2 Institute of Animal Science, Ningxia Academy of Agriculture and Forestry Sciences, Yinchuan 750021
  • Received:2023-08-07 Accepted:2023-09-25 Online:2024-03-25 Published:2024-03-25
  • Contact: WEI DaWei

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Abstract:

【Objective】 Skeletal muscle is an important component of animal body, and its growth and development directly affect the meat yield of livestock and poultry. As an important transcription regulator, fork head box protein O1 (FoxO1) is closely related to the growth and development of skeletal muscle. Exploring the effects of overexpression of FoxO1 gene on the proliferation, apoptosis and differentiation of bovine skeletal muscle cells could provide the theoretical basis for genetic improvement of beef. 【Method】 The tissue expression profile of FoxO1 was constructed by real-time fluorescence quantitative PCR (qPCR). To test the cell differentiation performance of bovine skeletal muscle cells which were isolated by enzyme digestion, the myotubes formation was observed and the expressions of differentiation marker genes were detected by qPCR. The subcellular localization of bovine skeletal muscle cells was carried out by immunofluorescence technique. In order to improve the expression of FoxO1 in bovine skeletal muscle cells, bovine FoxO1 overexpression adenovirus were designed and packaged. The effect of FoxO1 overexpression on the relative proliferation rate of cells was detected by EdU staining. Flow cytometry was used to detect the effect of FoxO1 overexpression on cell cycle distribution. The effects of FoxO1 overexpression on the expression levels of genes related to proliferation, apoptosis and differentiation of bovine skeletal muscle cells were investigated by qPCR.【Result】 The results of tissue expression spectrum showed that FoxO1 was expressed in many tissues, with the highest expression in the back fat of adult cattle and the lowest expression in the longissimus dorsi muscle tissue, while the expression of FoxO1 in the longissimus dorsi muscle tissue of calves was significantly higher than that of adult cattle (P<0.01). The results of subcellular localization showed that FoxO1 was expressed in the nucleus and cytoplasm of bovine skeletal muscle cells, and the fluorescence intensity in the nucleus was higher than that in the cytoplasm. The FoxO1 overexpression vector was successfully constructed, and the packaging and propagation of FoxO1 recombinant adenovirus were completed. After infecting bovine skeletal muscle cells, the FoxO1 expression level was significantly improved (P<0.01). EdU detection showed that overexpression of FoxO1 significantly reduced the cell proliferation rate (P<0.01), and flow cytometry showed that overexpression of FoxO1 significantly increased the number of cells in G1 phase and decreased the number of cells in S phase and G2 phase, inhibited the transformation of cells in G1/S phase and reduced the formation of cells in G2 phase. Further detection by qPCR found that the proliferation-related genes of PCNA, CDK1, CDK2, CCNA2, CCNB1, CCND1 and CCNE2 were significantly down-regulated (P<0.01), the apoptosis-related genes BAD and BAX were significantly up-regulated, and the apoptosis-inhibiting gene BCL2 was significantly down-regulated (P<0.05). After FoxO1 was overexpressed, the myotube formation of bovine skeletal muscle cells decreased, and the expression levels of MYOD, MYOG, MYF5, MYF6 and MYHC related to skeletal muscle differentiation were significantly decreased by qPCR detection (P<0.05). 【Conclusion】 FoxO1 was expressed in different tissues of cattle, and it was a ubiquitous transcription regulator. There were differences in expression at different stages of the growth and development of longissimus dorsi muscle, which played a role in stage regulation. FoxO1 played a transcriptional regulatory role in both the nucleus and cytoplasm, especially in the nucleus. Overexpression of FoxO1 might inhibit the proliferation and differentiation of bovine skeletal muscle cells by inhibiting the expression of genes related to cell proliferation and muscle cell differentiation, and might promote the apoptosis of bovine skeletal muscle cells by up-regulating the expression of apoptosis-promoting genes and down-regulating the expression of apoptosis- inhibiting genes.

Key words: FoxO1, bovine skeletal muscle cells, proliferation, differentiation

Table 1

Primers for real-time quantitative PCR (qPCR)"

基因名称
Gene name		 引物序列
Primer sequence (5′→3′)		 产物长度
Products length (bp)		 基因登录号
Genbank ID
GAPDH F：CCAACGTGTCTGTTGTGGAT 80 NM_001034034
R：CTGCTTCACCACCTTCTTGA
FoxO1 F：GCAGATTTACGAGTGGATGG 86 XM_025000053.1
R：TTGAATTCTTCCAGCCCG
PCNA F：GAACCTCACCAGCATGTCCA 97 NM_001034494
R：TACTAGTGCCAACGTGTCCG
CDK1 F：GAAGGGGTTCCTAGTACTGC 176 NM_174016
R：ATGAACTGACCAGGAGGG
CDK2 F：GCCAGGAGTTACTTCTATGC 102 NM_001014934
R：CTCCGTCCATCTTCATCC
CCNA2 F：ACACAGTCACAGGACAAAGC 107 NM_001075123
R：TCTGAGGTAGGTCTGGTGAA
CCNB1 F：TGGAGAGGTTGATGTTGAGC 95 NM_001045872
R：TCTGAGAAGGAGGAAAGTGC
CCND1 F：TCCTCTCCTATCACCGCCTGAC 175 NM_001046273
R：ACCTCCTCCTCCTCCTCTTCCT
CCNE2 F：GCTTATGTCACTGATGGTGCTTG 112 NM_001015665
R：TTAGCCAGGAGATGACCGTTAC
MYOD F：GGCCGCTGTTTACTGTGGG 162 NM_001040478
R：CAGCCGCTGGTTTGGGTT
MYOG F：CTATGACGGGGAGAACTACCTG 249 NM_001111325
R：CATTCACCTTCTTGAGTCTGCG
MYHC F：GCCCACTTCTCCCTCATTCACT 201 XM_010815980
R：ACCCTTCTTCTTGCCACCTTTC
MYF5 F：CTCTGATGGCATGCCTGAATGT 180 NM_174116
R：GGCAATCCAGGTTGCTCTGA
MYF6 F：TGGACCCCTTCAGCTACAGAC 126 NM_181811
R：CTTCCTTGGCAGTTATCACGAG
BAX F：GAGATGAATTGGACAGTAACA 118 NM_173894
R：TTGAAGTTGCCGTCAGAA
BAD F：CTCAGCAAGCACTGGCTAACA 270 NM_001035459
R：GTGAAACTCGTCGCTCATCCT
BCL2 F：TTAGCCAGTGCTTGCTGAGAC 86 NM_001166486
R：TTAGCCAGTGCTTGCTGAGAC

Table 2

Primer information"

基因名称
Gene name		 引物方向
Primer direction		 引物序列
Primer sequence (5′→3′)		 产物长度
Products length (bp)		 基因登录号
Genbank ID
FoxO1 F-Kpn I-FoxO1 CGGGGTACCGCCACCATGGCCGAAGCGCCCCAGGTG 1998 XM_025000053.1
R-Hind IlI-FoxO1 CCCAAGCTTTCAGCCTGACACCCAGCTGTGTG

Fig. 1

Tissue expression profile of FoxO1 A: Relative expression of FoxO1 in different tissues of cattle; B: Expression of FoxO1 in the longissimus dorsi muscle of adult cattle and calves"

Fig. 2

Isolation, culture and induced differentiation of bovine skeletal muscle cells A: Cell separation for 1 day; B: Subculture of bovine skeletal muscle cells; C: Induced differentiation for 4 d, 40×"

Fig. 3

Detection of expression level of differentiation marker genes in skeletal muscle cells A: MYOD and MYF5 were expressed in the early stage of differentiation; B: MYOG, MYF6 and MYHC were expressed in the middle and late stage of differentiation"

Fig. 4

Subcellular localization of FoxO1 A: Immunofluorescence staining of FoxO1 antibody; B: DAPI staining; C: Merge image"

Fig. 5

Packaging process of P1 generation of FoxO1 overexpression virus"

Fig. 6

EdU detected the effect of FoxO1 overexpression on the relative proliferation rate of bovine skeletal muscle cells A: EdU staining; B: Relative cell proliferation rate"

Fig. 7

Effect of FoxO1 overexpression on cell cycle distribution of bovine skeletal muscle cells detected by flow cytometry A: Cell cycle distribution was detected by flow cytometry; B: Statistical analysis of cell cycle distribution"

Fig. 8

The expression level of related genes was detected by qPCR A: Overexpression efficiency of FoxO1; B: Effects of FoxO1 overexpression on the expression level of proliferation and apoptosis relative genes in bovine skeletal muscle cells"

Fig. 9

Cell morphology of bovine skeletal muscle cells after induced differentiation in control group and experimental group A and B: Cell observation, 40×; C and D: Cell observation, 100×"

Fig. 10

Effects of FoxO1 overexpression on differentiation marker genes of bovine skeletal muscle cells A: Overexpression efficiency of FoxO1 gene after induced differentiation of bovine skeletal muscle cells; B: Detection of expression level of differentiation marker genes in bovine skeletal muscle cells"

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