. 2019 Jun 14;20(12):2923.

doi: 10.3390/ijms20122923.

Integrative Analyses of mRNA Expression Profile Reveal the Involvement of IGF2BP1 in Chicken Adipogenesis

Jiahui Chen^{1

2

3}, Xueyi Ren^{4

5

6}, Limin Li^{7

8

9}, Shiyi Lu^{10

11

12}, Tian Chen^{13

14

15}, Liangtian Tan^{16

17

18}, Manqing Liu^{19

20

21}, Qingbin Luo^{22

23

24}, Shaodong Liang^{25

26

27}, Qinghua Nie^{28

29

30}, Xiquan Zhang^{31

32

33}, Wen Luo^{34

35

36}

Affiliations

¹ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. Jiahui_CHEN@stu.scau.edu.cn.
² Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. Jiahui_CHEN@stu.scau.edu.cn.
³ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. Jiahui_CHEN@stu.scau.edu.cn.
⁴ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. xueyi_ren@stu.scau.edu.cn.
⁵ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. xueyi_ren@stu.scau.edu.cn.
⁶ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. xueyi_ren@stu.scau.edu.cn.
⁷ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. lilimin@stu.scau.edu.cn.
⁸ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. lilimin@stu.scau.edu.cn.
⁹ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. lilimin@stu.scau.edu.cn.
¹⁰ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. lushiyi@stu.scau.edu.cn.
¹¹ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. lushiyi@stu.scau.edu.cn.
¹² Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. lushiyi@stu.scau.edu.cn.
¹³ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. tian_cheng@stu.scau.edu.cn.
¹⁴ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. tian_cheng@stu.scau.edu.cn.
¹⁵ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. tian_cheng@stu.scau.edu.cn.
¹⁶ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. liangtian_tan@stu.scau.edu.cn.
¹⁷ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. liangtian_tan@stu.scau.edu.cn.
¹⁸ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. liangtian_tan@stu.scau.edu.cn.
¹⁹ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. liumanqing@scau.edu.cn.
²⁰ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. liumanqing@scau.edu.cn.
²¹ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. liumanqing@scau.edu.cn.
²² Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. qbluo@scau.edu.cn.
²³ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. qbluo@scau.edu.cn.
²⁴ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. qbluo@scau.edu.cn.
²⁵ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. sdliang@scau.edu.cn.
²⁶ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. sdliang@scau.edu.cn.
²⁷ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. sdliang@scau.edu.cn.
²⁸ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. nqinghua@scau.edu.cn.
²⁹ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. nqinghua@scau.edu.cn.
³⁰ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. nqinghua@scau.edu.cn.
³¹ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. xqzhang@scau.edu.cn.
³² Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. xqzhang@scau.edu.cn.
³³ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. xqzhang@scau.edu.cn.
³⁴ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. luowen729@scau.edu.cn.
³⁵ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. luowen729@scau.edu.cn.
³⁶ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. luowen729@scau.edu.cn.

PMID: 31208008
PMCID: PMC6627201
DOI: 10.3390/ijms20122923

Integrative Analyses of mRNA Expression Profile Reveal the Involvement of IGF2BP1 in Chicken Adipogenesis

Jiahui Chen et al. Int J Mol Sci. 2019.

. 2019 Jun 14;20(12):2923.

doi: 10.3390/ijms20122923.

Authors

Affiliations

¹ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. Jiahui_CHEN@stu.scau.edu.cn.
² Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. Jiahui_CHEN@stu.scau.edu.cn.
³ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. Jiahui_CHEN@stu.scau.edu.cn.
⁴ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. xueyi_ren@stu.scau.edu.cn.
⁵ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. xueyi_ren@stu.scau.edu.cn.
⁶ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. xueyi_ren@stu.scau.edu.cn.
⁷ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. lilimin@stu.scau.edu.cn.
⁸ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. lilimin@stu.scau.edu.cn.
⁹ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. lilimin@stu.scau.edu.cn.
¹⁰ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. lushiyi@stu.scau.edu.cn.
¹¹ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. lushiyi@stu.scau.edu.cn.
¹² Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. lushiyi@stu.scau.edu.cn.
¹³ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. tian_cheng@stu.scau.edu.cn.
¹⁴ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. tian_cheng@stu.scau.edu.cn.
¹⁵ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. tian_cheng@stu.scau.edu.cn.
¹⁶ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. liangtian_tan@stu.scau.edu.cn.
¹⁷ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. liangtian_tan@stu.scau.edu.cn.
¹⁸ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. liangtian_tan@stu.scau.edu.cn.
¹⁹ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. liumanqing@scau.edu.cn.
²⁰ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. liumanqing@scau.edu.cn.
²¹ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. liumanqing@scau.edu.cn.
²² Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. qbluo@scau.edu.cn.
²³ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. qbluo@scau.edu.cn.
²⁴ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. qbluo@scau.edu.cn.
²⁵ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. sdliang@scau.edu.cn.
²⁶ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. sdliang@scau.edu.cn.
²⁷ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. sdliang@scau.edu.cn.
²⁸ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. nqinghua@scau.edu.cn.
²⁹ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. nqinghua@scau.edu.cn.
³⁰ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. nqinghua@scau.edu.cn.
³¹ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. xqzhang@scau.edu.cn.
³² Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. xqzhang@scau.edu.cn.
³³ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. xqzhang@scau.edu.cn.
³⁴ Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou 510642, China. luowen729@scau.edu.cn.
³⁵ Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China. luowen729@scau.edu.cn.
³⁶ Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou 510642, China. luowen729@scau.edu.cn.

PMID: 31208008
PMCID: PMC6627201
DOI: 10.3390/ijms20122923

Abstract

Excessive abdominal fat deposition is an issue with general concern in broiler production, especially for Chinese native chicken breeds. A high-fat diet (HFD) can induce body weight gained and excessive fat deposition, and genes and pathways participate in fat metabolism and adipogenesis would be influenced by HFD. In order to reveal the main genes and pathways involved in chicken abdominal fat deposition, we used HFD and normal diet (ND) to feed a Chinese native chicken breed, respectively. Results showed that HFD can increase abdominal fat deposition and induce adipocyte hypertrophy. Additionally, we used RNA-sequencing to identify the differentially expressed genes (DEGs) between HFD and ND chickens in liver and abdominal fat. By analyzed these DEGs, we found that the many DEGs were enriched in fat metabolism related pathways, such as peroxisome proliferator-activated receptor (PPAR) signaling, fat digestion and absorption, extracellular matrix (ECM)-receptor interaction, and steroid hormone biosynthesis. Notably, the expression of insulin-like growth factor II mRNA binding protein 1 (IGF2BP1), which is a binding protein of IGF2 mRNA, was found to be induced in liver and abdominal fat by HFD. Ectopic expression of IGF2BP1 in chicken liver-related cell line Leghorn strain M chicken hepatoma (LMH) cell revealed that IGF2BP1 can regulate the expression of genes associated with fatty acid metabolism. In chicken preadipocytes (ICP cell line), we found that IGF2BP1 can promote adipocyte proliferation and differentiation, and the lipid droplet content would be increased by overexpression of IGF2BP1. Taken together, this study provides new insights into understanding the genes and pathways involved in abdominal fat deposition of Chinese native broiler, and IGF2BP1 is an important candidate gene for the study of fat metabolism and adipogenesis in chicken.

Keywords: Chinese native broiler; IGF2BP1; abdominal fat deposition; adipogenesis; differentially expressed gene; high-fat diet.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

**Figure 1**
High-fat diet promotes chicken abdominal fat deposition and induces adipocyte hypertrophy. (a) Body weight of the broilers fed with high-fat diet (HFD) and normal diet (ND). (b) Abdominal fat weight of the broilers fed with HFD and ND. (c) Abdominal fat rate of the broilers fed with HFD and ND. (d) Micrograph of abdominal fat cross-section from HFD (left) and ND (right) chickens. Bar, 200 µm. (e) Area (left) and diameter (right) of the adipocyte from HFD and ND chicken abdominal fat. * p < 0.05; ** p < 0.01.

**Figure 2**
Differentially expressed genes between HFD and ND chickens. (a) Scatter plot of differentially expressed genes (DEGs) between HFD and ND chickens in abdominal fat. (b) Scatter plot of DEGs between HFD and ND chickens in liver. (c) Enriched Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway of DEGs between HFD and ND chickens in abdominal fat. (d) Enriched KEGG pathway of DEGs between HFD and ND chickens in liver. (e) Gene Ontology (GO) enrichment of DEGs between HFD and ND chickens in abdominal fat. (f) GO enrichment of DEGs between HFD and ND chickens in liver.

**Figure 3**
The expression of *IGF2BP1* can be significantly induced in a high-fat condition. (a) Specific and common DEGs in liver and abdominal fat. The three groups of the Venn diagram represent the liver specific DEGs between HFD and ND chicken (blue), common DEGs between HFD and ND chicken in liver and abdominal fat (deep red), and abdominal fat specific DEGs between HFD and ND chicken (light red), respectively. (b) RNA-sequencing revealed that HFD can significantly induce *IGF2BP1* expression in liver and abdominal fat of chicken. (c) qPCR validation of six DEGs obtained from RNA-seq in liver. (d) qPCR validation of 6 DEGs obtained from RNA-seq in abdominal fat. (e). High-fat medium can significantly promote *IGF2BP1* expression in chicken LMH cell. (f) High-fat medium can significantly promote *IGF2BP1* expression in chicken ICP cell. The data are mean ± S.E.M. with four samples (Figure 3b has three samples). Independent sample t-test was used to analyze the statistical differences between groups. * p < 0.05; ** p < 0.01.

**Figure 4**
*IGF2BP1* promotes the expression of genes involved in fatty acid metabolism in LMH cell. (a) The mRNA expression of *IGF2BP1* after 48 h transfection of si-IGF2BP1 in LMH cell. (b) The protein expression of *IGF2BP1* after 48 h transfection of si-IGF2BP1 in LMH cell. (c) The mRNA expression of *IGF2BP1* after 48 h transfection of *IGF2BP1* overexpression vector in LMH cell. (d) The protein expression of *IGF2BP1* after 48 h transfection of *IGF2BP1* overexpression vector in LMH cell. (e) The expression of genes related to fatter acid metabolism after transfection of si-IGF2BP1 in LMH cell. (f) The expression of genes related to fatter acid metabolism after transfection of pcDNA3.1-IGF2BP1 in LMH cell. The data are mean ± S.E.M. with four samples (n = 4/treatment group). Independent sample t test was used to analyze the statistical differences between groups. * p < 0.05; ** p < 0.01.

**Figure 5**
*IGF2BP1* promotes chicken adipocyte proliferation. (a) The mRNA and protein expression of *IGF2BP1* after 48 h transfection of si-IGF2BP1 in an ICP cell. (b) The mRNA and protein expression of *IGF2BP1* after 48 h transfection of *IGF2BP1* overexpression vector in an ICP cell. (c). The expression of cell cycle related genes after transfection of si-IGF2BP1 in an ICP cell. (d) The expression of cell cycle related genes after overexpression of *IGF2BP1* in an ICP cell. (e) *IGF2BP1* inhibition induced cell cycle arrest in an ICP cell. (f) *IGF2BP1* overexpression promote cell cycle progress in an ICP cell. (g) *IGF2BP1* inhibition repressed cell proliferation in an ICP cell. (h) *IGF2BP1* overexpression promote cell proliferation in an ICP cell. The data are mean ± S.E.M. with at least 3 samples (n ≥ 3/treatment group). Independent sample t test was used to analyze the statistical differences between groups. * p < 0.05; ** p < 0.01.

**Figure 6**
*IGF2BP1* promotes chicken adipocyte differentiation and increases lipid droplet accumulation. (a) The expression of *IGF2BP1* during ICP cell differentiation. (b) The expression of genes related to adipocyte differentiation and fatty acid metabolism after *IGF2BP1* overexpression in an ICP cell. (c). The expression of genes related to adipocyte differentiation and fatty acid metabolism after inhibition of *IGF2BP1* expression in an ICP cell. (d). Representative images of oil red O staining (red) after overexpression of *IGF2BP1* in an ICP cell; scale bar: 100 μm. (e). Lipid droplet content by oil red O staining and extraction method of cells transfected with *IGF2BP1* overexpression vector. (f). Representative images of oil red O staining (red) after inhibition of *IGF2BP1* in an ICP cell; scale bar: 100 μm. (g). Lipid droplet content by oil red O staining and extraction method of cells transfected with si-IGF2BP1 and si-NC. The data are mean ± S.E.M. with four samples (n = 4/treatment group). Independent sample t test was used to analyze the statistical differences between groups. * p < 0.05; ** p < 0.01.

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Integrative Analyses of mRNA Expression Profile Reveal the Involvement of IGF2BP1 in Chicken Adipogenesis

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Integrative Analyses of mRNA Expression Profile Reveal the Involvement of IGF2BP1 in Chicken Adipogenesis

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