Journal of Zhejiang University-SCIENCE B

, Volume 18, Issue 6, pp 492–500 | Cite as

CIDE gene expression in adipose tissue, liver, and skeletal muscle from obese and lean pigs

  • Yue-qin Qiu
  • Xue-fen YangEmail author
  • Xian-yong Ma
  • Yun-xia Xiong
  • Zhi-mei Tian
  • Qiu-li Fan
  • Li Wang
  • Zong-yong Jiang


The expression of the cell death-inducing DNA fragmentation factor α-like effector (CIDE) family including Cidea, Cideb, and Cidec was significantly increased in mouse and human models of obesity. However, there was less information on these genes’ expression in pigs. Here, we hypothesized that different fat accumulation between lean (Duroc×Landrace×Yorkshire gilts, DLY) and obese (Lantang) pigs was attributed to porcine CIDE-modulating lipid metabolism. Our data showed that Cidea and Cidec were expressed at a high level in adipose tissue, and at a relatively high level in skeletal muscle, whereas Cideb was mainly expressed in the liver in both breeds of pig. Lantang pigs had higher white adipose and skeletal muscle Cidea and Cidec mRNA abundance, and hepatic and muscle Cideb mRNA than DLY pigs. Lipid metabolism-related genes including sterol regulatory element binding protein 1c (SREBP-1c), hepatocyte nuclear factor-4α (HNF-4α), peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α), fatty acid synthase (FASN), diacylglycerol O-acyltransferase 1 (DGAT1), and DGAT2 showed a higher expression level in adipose tissue from obese pigs than in that from lean pigs. Lantang pigs exhibited higher mRNA abundance for liver SREBP-1c, HNF-4α, and PGC-1α, and higher skeletal muscle SREBP-1c, HNF-4α, PGC-1α, and DGAT2 expression, as compared with DLY pigs. However, the perlipin2 mRNA levels in adipose tissues, liver, and skeletal muscle were significantly lower in obese pigs than in their lean counterparts. Furthermore, plasma non-esterified fatty acid (NEFA), glucose, and triacylglycerol (TAG) levels were greater in obese pigs than in lean pigs. Finally, data from correlation analysis further found that CIDE mRNA expression was positively correlated with back fat thickness (BFT), abdominal fat mass (AFM), and the levels of NEFA, TAG, and glucose in the two breeds. Collectively, these data revealed that the porcine CIDEs possibly modulated lipid metabolism and contributed to the development of fat deposition and obesity in Lantang pigs.

Key words

Cell death-inducing DNA fragmentation factor α-like effector (CIDE) Adipose tissue Liver Skeletal muscle Fat deposition Lantang pig DLY pig 

肥胖型和瘦肉型猪的脂肪、肝脏及骨骼肌组织中 CIDE 家族基因表达水平的比较研究



研究CIDE 家族基因在肥胖型和瘦肉型猪的脂肪、 肝脏及肌肉组织中的基因表达水平差异,并初步 探CIDE 家族基因与脂质代谢的关系。


首次在肥胖型与瘦肉型猪模型中解释CIDE 家族 基因可以调节脂质代谢,并有助于脂肪沉积及导 致肥胖。


采用荧光定量聚合酶链式反应(qPCR)检测肥胖 型蓝塘猪和瘦肉型杜长大猪的脂肪、肝脏和骨骼 肌中CIDE 家族基因、SREBP-1c、PGC-1α、 HNF-4α、FASN、DGAT1DGAT2、perlipin 2 等基因表达水平。采用血浆生化指标仪试剂盒检 测两个品种猪血浆中甘油三酯、葡萄糖、游离脂 肪酸及胆固醇的含量。


肥胖型蓝塘猪脂肪和背最长肌组织中的Cidea 和 Cidec,及肝脏中Cidec 的基因表达量明显高于瘦 肉型杜长大猪。在脂肪组织中,脂质代谢相关的 基因(包括SREBP-1c、PGC-1α、HNF-4α、FASN、 DGAT1 和DGAT2 基因)表达量都是蓝塘猪高于 杜长大猪。蓝塘猪肝脏中的SREBP-1c、HNF-4αPGC-1α 基因表达水平显著高于杜长大猪。蓝 塘猪背最长肌组织的SREBP-1c 、HNF-4α 、 PGC-1α 和DGAT2 基因表达量高于杜长大猪。然 而,蓝塘猪的脂肪、肝脏及背最长肌三种组织中 的perlipin 2 的表达量显著低于杜长大猪。此外, 蓝塘猪血浆中的甘油三酯、葡萄糖及游离脂肪酸 浓度明显高于杜长大猪。通过相关性分析,我们 发现肥胖型和瘦肉型猪不同组织中的CIDE 家族 基因表达水平与背部脂肪厚度、腹部脂肪重量、 血浆中的甘油三酯、葡萄糖及游离脂肪酸浓度有 明显的正向相关性。综上所述,CIDE 家族基因 可以调节脂质代谢,并促进脂肪沉积及导致肥胖。


CIDE家族基因 脂肪沉积 脂肪 肝脏 骨骼肌 蓝塘猪 杜长大猪 

CLC number



Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abu-Elheiga, L., Oh, W., Kordari, P., et al., 2003. Acetyl-CoA carboxylase 2 mutant mice are protected against obesity and diabetes induced by high-fat/high-carbohydrate diets. Proc. Natl. Acad. Sci. USA, 100(18):10207–10212. Scholar
  2. Ahima, R.S., Flier, J.S., 2000. Adipose tissue as an endocrine organ. Trends Endocrinol. Metab., 11(8):327–332. Scholar
  3. Bell, M., Wang, H., Chen, H., et al., 2008. Consequences of lipid droplet coat protein downregulation in liver cells: abnormal lipid droplet metabolism and induction of insulin resistance. Diabetes, 57(8):2037–2045. Scholar
  4. Bernlohr, D.A., Jenkins, A.E., Bennaars, A.A., 2002. Adipose tissue and lipid metabolism. In: Vance, D.E., Vance, J.E. (Eds.), Biochemistry of Lipids, Lipoproteins and Membranes, 4th Ed. Elsevier, Amsterdam, p.263–289. Scholar
  5. Chen, Z.J., Norris, J.Y., Finck, B.N., 2010. Peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) stimulates VLDL assembly through activation of cell death-inducing DFFA-like effector B (CideB). J. Biol. Chem., 285(34):25996–26004. Scholar
  6. Chen, Z.M., Qi, X.H., Zhang, H., et al., 2010. Changes of leptin and leptin receptor gene expression in subcutaneous fat and hypothalamus of Lantang and Landrace pigs. J. Huazhong Agric. Univ., 29(1):67–70 (in Chinese).Google Scholar
  7. Danesch, U., Hoeck, W., Ringold, G.M., 1992. Cloning and transcriptional regulation of a novel adipocyte-specific gene, FSP27. CAAT-enhancer-binding protein (C/EBP) and C/EBP-like proteins interact with sequences required for differentiation-dependent expression. J. Biol. Chem., 267(10):7185–7193.PubMedGoogle Scholar
  8. Girousse, A., Langin, D., 2012. Adipocyte lipases and lipid droplet-associated proteins: insight from transgenic mouse models. Int. J. Obes. (Lond.), 36(4):581–594. Scholar
  9. Gong, J., Sun, Z., Li, P., 2009. CIDE proteins and metabolic disorders. Curr. Opin. Lipidol., 20(2):121–126. Scholar
  10. Hallberg, M., Morganstein, D.L., Kiskinis, E., et al., 2008. A functional interaction between RIP140 and PGC-1a regulates the expression of the lipid droplet protein CIDEA. Mol. Cell. Biol., 28(22):6785–6795. Scholar
  11. Herzig, S., Long, F., Jhala, U.S., et al., 2001. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature, 413(6852):179–183. Scholar
  12. Horton, J.D., Goldstein, J.L., Brown, M.S., 2002. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest., 109(9): 1125–1131. Scholar
  13. Hulver, M.W., Berggren, J.R., Cortright, R.N., et al., 2003. Skeletal muscle lipid metabolism with obesity. Am. J. Physiol. Endocrinol. Metab., 284(4):E741–E747. Scholar
  14. Inohara, N., Koseki, T., Chen, S., et al., 1998. CIDE, a novel family of cell death activators with homology to the 45 kDa subunit of the DNA fragmentation factor. EMBO J., 17(9):2526–2533. Scholar
  15. Jiang, J.P., Zhou, J., Chen, J., et al., 2007. Effect of chicken egg yolk antibody against adipose tissue plasma membranes on carcass composition and lipogenic hormones and enzymes in pigs. Livestock Sci., 107(2-3):235–243. Scholar
  16. Keller, P., Petrie, J.T., de Rose, P., et al., 2008. Fat-specific protein 27 regulates storage of triacylglycerol. J. Biol. Chem., 283(21):14355–14365. Scholar
  17. Lan, L.T., Huang, L.S., Ma, J.W., et al., 2004. Experiment for comparing the performance of Erhualian pig double cross combinations and that of Duroc×(Landrace×Large Yorkshire) three-way cross combination. J. Southwest Univ. Natl., 30(6):741–744.Google Scholar
  18. Leonhardt, M., Langhans, W., 2004. Fatty acid oxidation and control of food intake. Physiol. Behav., 83(4):645–651. Scholar
  19. Li, J.Z., Ye, J., Xue, B., et al., 2007. Cideb regulates dietinduced obesity, liver steatosis, and insulin sensitivity by controlling lipogenesis and fatty acid oxidation. Diabetes, 56(10):2523–2532. Scholar
  20. Li, J.Z., Lei, Y., Wang, Y., et al., 2010. Control of cholesterol biosynthesis, uptake and storage in hepatocytes by Cideb. Biochim. Biophys. Acta, 1801(5):577–586. Scholar
  21. Li, X.H., Ye, J., Zhou, L.K., et al., 2012. Opposing roles of cell death-inducing DFF45-like effector B and perilipin 2 in controlling hepatic VLDL lipidation. J. Lipid Res., 53(9): 1877–1889. Scholar
  22. Li, Y.H., Lei, T., Chen, X.D., et al., 2009. Molecular cloning, chromosomal location and expression pattern of porcine CIDEa and CIDEc. Mol. Biol. Rep., 36(3):575–582. Scholar
  23. Liu, Y., Millar, J.S., Cromley, D.A., et al., 2008. Knockdown of Acyl-CoA: diacylglycerol acyltransferase 2 with antisense oligonucleotide reduces VLDL TGand ApoB secretion in mice. Biochim. Biophys. Acta, 1781(3):97–104. Scholar
  24. Lu, P., Li, D.F., Yin, J.D., et al., 2008. Flavour differences of cooked longissimus muscle from Chinese indigenous pig breeds and hybrid pig breed (Duroc×Landrace×Large White). Food Chem., 107(4):1529–1537. Scholar
  25. Malaguarnera, M., Di Rosa, M., Nicoletti, F., et al., 2009. Molecular mechanisms involved in NAFLD progression. J. Mol. Med. (Berl.), 87(7):679–695. Scholar
  26. Nishino, N., Tamori, Y., Tateya, S., et al., 2008. FSP27 contributes to efficient energy storage in murine white adipocytes by promoting the formation of unilocular lipid droplets. J. Clin. Invest., 118(8):2808–2821. Scholar
  27. Nishizuka, Y., 1992. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase. Science, 258(5082):607–614. Scholar
  28. Nordström, E.A., Rydén, M., Backlund, E.C., et al., 2005. A human-specific role of cell death-inducing DFFA (DNA fragmentation factor-a)-like effector A (CIDEA) in adipocyte lipolysis and obesity. Diabetes, 54(6):1726–1734. Scholar
  29. O'Hea, E.K., Leveille, G.A., 1969. Significance of adipose tissue and liver as sites of fatty acid synthesis in the pig and the efficiency of utilization of various substrates for lipogenesis. J. Nutr., 99(3):338–344.PubMedGoogle Scholar
  30. Shimomura, I., Bashmakov, Y., Horton, J.D., 1999. Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J. Biol. Chem., 274(4):30028–30032. Scholar
  31. Singaravelu, R., Lyn, R.K., Srinivasan, P., et al., 2013. Human serum activates CIDEB-mediated lipid droplet enlargement in hepatoma cells. Biochem. Biophys. Res. Commun., 441(2):447–452. Scholar
  32. Tian, Z.M., Ma, X.Y., Yang, X.F., et al., 2016. Influence of low protein diets on gene expression of digestive enzymes and hormone secretion in the gastrointestinal tract of young weaned piglets. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 17(10):742–751. Scholar
  33. Toh, S.Y., Gong, J., Du, G., et al., 2008. Up-regulation of mitochondrial activity and acquirement of brown adipose tissue-like property in the white adipose tissue of Fsp27 deficient mice. PLoS ONE, 3(8):e2890. Scholar
  34. Vandesompele, J., de Preter, K., Pattyn, F., et al., 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol., 3(7):research0034.1. Scholar
  35. Walstra, P., Merkus, G.S.M., 1995. Procedure for assessment of the lean meat percentage as a consequence of the new EUreference dissection method in pig carcass classification. Report ID-DLO 96.014, Zeist, the Netherlands.Google Scholar
  36. Yonezawa, T., Kurata, R., Kimura, M., et al., 2011. Which CIDE are you on? Apoptosis and energy metabolism. Mol. Biosyst., 7(1):91–100. Scholar
  37. Yu, M., Wang, H., Zhao, J., et al., 2013. Expression of CIDE proteins in clear cell renal cell carcinoma and their prognostic significance. Mol. Cell. Biochem., 378(1): 145–151. Scholar
  38. Zhou, Z., Yon Toh, S., Chen, Z., et al., 2003. Cidea-deficient mice have lean phenotype and are resistant to obesity. Nat. Genet., 35(1):49–56. Scholar

Copyright information

© Zhejiang University and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Yue-qin Qiu
    • 1
  • Xue-fen Yang
    • 1
    Email author
  • Xian-yong Ma
    • 1
  • Yun-xia Xiong
    • 1
  • Zhi-mei Tian
    • 1
  • Qiu-li Fan
    • 1
  • Li Wang
    • 1
  • Zong-yong Jiang
    • 1
  1. 1.Ministry of Agriculture Key Laboratory of Animal Nutrition and Feed Science in South China, State Key Laboratory of Livestock and Poultry Breeding, Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangdong Key Laboratory of Animal Breeding and Nutrition, Institute of Animal ScienceGuangdong Academy of Agricultural SciencesGuangzhouChina

Personalised recommendations