The liver transcriptome of two full-sibling Songliao black pigs with extreme differences in backfat thickness

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Abstract

Background

Fatness traits in animals are important for their growth, meat quality, reproductive performance, and immunity. The liver is the principal organ of the regulation of lipid metabolism, and this study used massive parallelized high-throughput sequencing technologies to determine the porcine liver tissue transcriptome architecture of two full-sibling Songliao black pigs harboring extremely different phenotypes of backfat thickness.

Results

The total number of reads produced for each sample was in the region of 53 million, and 8,226 novel transcripts were detected. Approximately 92 genes were differentially regulated in the liver tissue, while 31 spliced transcripts and 33 primary transcripts showed significantly differential expression between pigs with higher and lower backfat thickness. Genes that were differentially expressed were involved in the metabolism of various substances, small molecule biochemistry, and molecular transport.

Conclusions

Genes involved in the regulation of lipids could play an important role in lipid and fatty acid metabolism in the liver. These results could help us understand how liver metabolism affects the backfat thickness of pigs.

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Most cited references 21

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The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance.

Qing-Wu Yan, Qin Yang, Nimesh Mody … (2007)

We identified lipocalin 2 (Lcn2) as a gene induced by dexamethasone and tumor necrosis factor-alpha in cultured adipocytes. The purpose of this study was to determine how expression of Lcn2 is regulated in fat cells and to ascertain whether Lcn2 could be involved in metabolic dysregulation associated with obesity. We examined Lcn2 expression in murine tissues and in 3T3-L1 adipocytes in the presence and absence of various stimuli. We used quantitative Western blotting to observe Lcn2 serum levels in lean and obese mouse models. To assess effects on insulin action, we used retroviral delivery of short hairpin RNA to reduce Lcn2 levels in 3T3-L1 adipocytes. Lcn2 is highly expressed by fat cells in vivo and in vitro. Expression of Lcn2 is elevated by agents that promote insulin resistance and is reduced by thiazolidinediones. The expression of Lcn2 is induced during 3T3-L1 adipogenesis in a CCAAT/enhancer-binding protein-dependent manner. Lcn2 serum levels are elevated in multiple rodent models of obesity, and forced reduction of Lcn2 in 3T3-L1 adipocytes improves insulin action. Exogenous Lcn2 promotes insulin resistance in cultured hepatocytes. Lcn2 is an adipokine with potential importance in insulin resistance associated with obesity.

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The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages.

Xiaoli Chen, Derek LeRoith, David A. Bernlohr … (2008)

Adipose tissue-derived cytokines (adipokines) are associated with the development of inflammation and insulin resistance. However, which adipokine(s) mediate this linkage and the mechanisms involved during obesity is poorly understood. Through proteomics and microarray screening, we recently identified lipocalin 2 (LCN 2) as an adipokine that potentially connects obesity and its related adipose inflammation. Herein we show that the levels of LCN2 mRNA are dramatically increased in adipose tissue and liver of ob/ob mice and primary adipose cells isolated from Zucker obese rats, and thiazolidinedione administration reduces LCN2 expression. Interestingly, addition of LCN2 induces mRNA levels of peroxisome proliferator-activated receptor-gamma (PPARgamma) and adiponectin. Reducing LCN2 gene expression causes decreased expression of PPARgamma and adiponectin, slightly reducing insulin-stimulated Akt2 phosphorylation at Serine 473 in 3T3-L1 adipocytes. LCN2 administration to 3T3-L1 cells attenuated TNFalpha-effect on glucose uptake, expression of PPARgamma, insulin receptor substrate-1, and glucose transporter 4, and secretion of adiponectin and leptin. When added to macrophages, LCN2 suppressed lipopolysaccharide-induced cytokine production. Our data suggest that LCN2, as a novel autocrine and paracrine adipokine, acts as an antagonist to the effect of inflammatory molecules on inflammation and secretion of adipokines.

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Fatty acids and hypolipidemic drugs regulate peroxisome proliferator-activated receptors alpha - and gamma-mediated gene expression via liver fatty acid binding protein: a signaling path to the nucleus.

F Spener, M Borrmann-Hassenbach, C Wolfrum … (2001)

Peroxisome proliferator-activated receptor alpha (PPARalpha) is a key regulator of lipid homeostasis in hepatocytes and target for fatty acids and hypolipidemic drugs. How these signaling molecules reach the nuclear receptor is not known; however, similarities in ligand specificity suggest the liver fatty acid binding protein (L-FABP) as a possible candidate. In localization studies using laser-scanning microscopy, we show that L-FABP and PPARalpha colocalize in the nucleus of mouse primary hepatocytes. Furthermore, we demonstrate by pull-down assay and immunocoprecipitation that L-FABP interacts directly with PPARalpha. In a cell biological approach with the aid of a mammalian two-hybrid system, we provide evidence that L-FABP interacts with PPARalpha and PPARgamma but not with PPARbeta and retinoid X receptor-alpha by protein-protein contacts. In addition, we demonstrate that the observed interaction of both proteins is independent of ligand binding. Final and quantitative proof for L-FABP mediation was obtained in transactivation assays upon incubation of transiently and stably transfected HepG2 cells with saturated, monounsaturated, and polyunsaturated fatty acids as well as with hypolipidemic drugs. With all ligands applied, we observed strict correlation of PPARalpha and PPARgamma transactivation with intracellular concentrations of L-FABP. This correlation constitutes a nucleus-directed signaling by fatty acids and hypolipidemic drugs where L-FABP acts as a cytosolic gateway for these PPARalpha and PPARgamma agonists. Thus, L-FABP and the respective PPARs could serve as targets for nutrients and drugs to affect expression of PPAR-sensitive genes.

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Author and article information

Contributors

Kai Xing

Feng Zhu

Liwei Zhai

Huijie Liu

Zhijun Wang

Zhuocheng Hou

Chuduan Wang

Journal

Journal ID (nlm-ta): J Anim Sci Biotechnol

Journal ID (iso-abbrev): J Anim Sci Biotechnol

Title: Journal of Animal Science and Biotechnology

Publisher: BioMed Central

ISSN (Print): 1674-9782

ISSN (Electronic): 2049-1891

Publication date Collection: 2014

Publication date (Electronic): 6 June 2014

Volume: 5

Issue: 1

Page: 32

Affiliations

[1 ]National Engineering Laboratory for Animal Breeding and MOA Key Laboratory of Animal Genetics and Breeding, Department of Animal Genetics and Breeding, China Agricultural University, 100193 Beijing, China

[2 ]Tianjin Ninghe Primary Pig Breeding Farm, Ninghe 301500, Tianjin, China

Article

Publisher ID: 2049-1891-5-32

DOI: 10.1186/2049-1891-5-32

PMC ID: 4106230

SO-VID: 60fdb09c-e513-45de-a199-0000003748a5

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

The liver transcriptome of two full-sibling Songliao black pigs with extreme differences in backfat thickness

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Abstract

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Results

Conclusions

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Animal models of intrauterine growth restriction (IUGR)

Most cited references 21

The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance.

The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages.

Fatty acids and hypolipidemic drugs regulate peroxisome proliferator-activated receptors alpha - and gamma-mediated gene expression via liver fatty acid binding protein: a signaling path to the nucleus.

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