Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (18): 3704-3718.doi: 10.3864/j.issn.0578-1752.2024.18.015

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles    

Research on the Regulatory Effects of Bovine Skeletal Muscle Cells on Adipocytes Under Co-Culture Conditions

YANG DongMei1(), ZHANG JiuPan2, SONG YaPing1, SONG XiaoYu1, JIANG Chao1, MA Yun1, 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:2023-03-19 Accepted:2024-06-03 Online:2024-09-16 Published:2024-09-29
  • Contact: WEI DaWei

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Abstract:

【Objective】 Marbling is one of the key indicators for meat quality, formed by the joint development of bovine skeletal muscle cells and bovine adipocytes. The purpose of this study was to simulate the interaction effect of bovine skeletal muscle cells and adipocytes in the process of meat formation in vivo to the greatest extent, and to establish two cell co-culture systems in vitro to explore the regulatory effects of bovine skeletal muscle cell secretion and metabolic factors on adipocytes under the co-culture system.【Method】 Bovine adipocytes and skeletal muscle cells were isolated separately using tissue block and enzymatic digestion methods. Cells were identified for purity and differentiation potential by phenotypic identification and gene expression profiling, the conditioned medium exchange co-cultivation systems constructed further, and Transwell co-cultivation systems involving bovine skeletal muscle cells and bovine fat cells was conducted. The impact of secretory and metabolic products from bovine skeletal muscle cells on the proliferation and differentiation of fat cells under co-culture conditions was assessed using techniques, such as real-time quantitative PCR (qPCR), EdU staining, and Oil Red O staining. 【Result】 In this study, two co-culture systems of bovine skeletal muscle cells and adipocytes were successfully constructed. Under the condition of medium exchange co-culture, the expression of bovine fat cell proliferation marker genes, including PCNA, CDK2, CCNE2, and CCND1, was significantly downregulated (P<0.01). Additionally, the expression of adipogenesis marker genes FABP4 and PPARγ was significantly decreased (P<0.05); the expression of LPL was greatly reduced (P<0.01). On the other hand, in the Transwell co-culture system, the expression of the bovine fat cell proliferation marker gene CCND1 was significantly downregulated (P<0.05); the expression of PCNA, CDK1, and CCNE2 was greatly downregulated (P<0.01). Additionally, the expression of the adipogenesis marker gene FABP4 was significantly decreased (P<0.05), while the expression of PPARγ, C/EBPβ, and LPL was extremely significantly decreased (P<0.01). 【Conclusion】 The results of this study indicated that secretory and metabolic products from bovine skeletal muscle cells could suppress the proliferation and differentiation of bovine adipocytes by inhibiting the expression of proliferation marker genes, including PCNA, CDK1, CDK2, CCNE2, and CCND1, as well as lipogenic marker genes, such as PPARγ, FABP4, CEBPβ, and LPL. The results of this study indicated that secretory and metabolic products from bovine skeletal muscle cells could suppress the proliferation and differentiation of bovine adipocytes by inhibiting the expression of proliferation marker genes, such as PCNA, CDK1, CDK2, CCNE2 and CCND1, as well as lipogenic marker genes, such as PPARγ, FABP4, CEBPβ and LPL.

Key words: cattle, adipocyte, skeletal muscle cells, co-culture, cell interactions

Table 1

The sequence infotmation of qPCR primers"

基因 Gene 引物序列Primer sequence(5'→3') 产物大小 Product length (bp) NCBI登录号 Genbank No.
PCNA F: GAACCTCACCAGCATGTCCA 97 NM_001034494
R: TACTAGTGCCAACGTGTCCG
CDK2 F: GCCAGGAGTTACTTCTATGC 102 NM_001014934.1
R: CTCCGTCCATCTTCATCC
CCNE2 F：GCTTATGTCACTGATGGTGCTTG 122 NM_001015665.1
R：TTAGCCAGGAGATGACCGTTAC
CCND1 F: TGGTCCTGGTGAACAAACTC 79 NM_176788
R: ATCTGCTTGTTCTCCTCGGC
C/EBPβ F: TTCCTCTCCGACCTCTTCTC 79 NM_176788
R: CCAGACTCACGTAGCCGTACT
FABP4 F: AAGTCAAGAGCATCGTAA 111 NM_174314.2
R: CCAGCACCATCTTATCAT
PPARγ F: AGGATGGGGTCCTCATATCC 121 NM_181024. 2
R: GCGTTGAACTTCACAGCAAA
LPL F: ACGATTATTGCTCAGCATGG 130 NM_001075120. 1
R: ACTTTGTACAGGCACAACCG
C/EBPα F: TGGACAAGAACAGCAACGAG 130 NM_176784
R: TTGTCACTGGTCAGCTCCAG
Myf6 F: ATTCCAGGGGGCTCGTGATA 107 NM_181811.2
R:CGAGGAAATGCTGTCCACGA
Myf5 F: CCATCCGCTACATTGAGAGT 179 NM_174116.1
R:GTAGACGCTGTCAAAACTGC
MyoG F: CCAGTACATAGAGCGCCTGC 183 NM_001111325.1
R: AGATGATCCCCTGGGTTGGG
GAPDH F:CCAACGTGTCTGTTGTGGAT 80 NM_001034034.2
R:CTGCTTCACCACCTTCTTGA

Table 2

qPCR reaction conditions"

反应程序
Reaction procedure		 温度
Temperature (℃)		 反应时间
Reaction time (s)
预变性 Pre-denaturation 95 30
变性 Denaturation 95 5
退火 Anneal 60 30
延伸 Extension 72 30

Fig. 1

Isolation, culture and identification of bovine adipocytes A: Separation 5 d; B: Separation 11 d; C: Bodipy staining; D: Oil red O staining; E: Expression of the lipogenic marker gene PPARγ; F: Expression of the fat-forming marker gene FABP4 * P<0.05， ** P<0.01，ns P>0.05. The same as below"

Fig. 2

Isolation, culture and identification of bovine skeletal muscle cells A: Separation of 0 d; B: Separation of 2 d; C: Induction of differentiation 2 d; D: Induction of differentiation 4 d; E: Expression of myoblastic marker gene Myf5; F: Expression of myoblastic marker gene Myf6; G: Expression of marker gene MyoG"

Fig. 3

Schematic illustration for the construction of a conditional co-culture medium model of bovine skeletal muscle cells and bovine adipocytes A: Proliferation system of conditional medium exchange co-culture system; B: Differentiation system of conditional medium exchange co-culture system; C: Proliferation system of Transwell co-culture system; D: Differentiation system of Transwell co-culture system"

Fig. 4

Morphological changes of bovine fat cells in the experimental group and control group under indirect co-culture conditions with a conditioned medium exchange A: Observation of cell morphology for each group after 2 days of co-culturing; B: Observation of cell morphology for each group after 4 days of co-culturing; C: Observation of cell morphology for each group after 6 days of co-culturing"

Fig. 5

Effect of conditioned media exchange co-culture on proliferation marker gene expression"

Fig. 6

Effect of conditioned medium exchange co-culture on adipogenic marker gene expression"

Fig. 7

Effects of conditioned medium exchange co-culture on proliferation and differentiation of bovine adipocytes A: EdU staining for 2 d co-culture of single cultured adipocytes and conditioned medium exchange; B: Cell proliferation rate"

Fig. 8

Effect of conditioned medium exchange co-culture on lipid droplet production in bovine adipocytes A: Lipid droplet staining of bovine adipocytes in monoculture and after conditioned medium exchange indirect co-culture; B: Counts of lipid droplets"

Fig. 9

Effects of Transwell co-culture on gene expression of proliferation markers"

Fig. 10

Effect of Transwell co-culture on adipogenic marker gene expression"

Fig. 11

Effects of Transwell co-culture on proliferation and differentiation of bovine adipocytes A: EdU staining of single-cultured adipocytes and Transwell co-culture for 2 d; B: Cell proliferation rate"

Fig. 12

Effect of Transwell co-culture on lipid droplet production in bovine adipocytes A: Lipid droplet staining of bovine adipocytes in monoculture and after Transwell indirect co-culturing.; B: Counts of lipid droplets"

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