Lysine 2-hydroxyisobutyrylation levels determined adipogenesis and fat accumulation in adipose tissue in pigs

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Abstract

Background

Excessive backfat deposition lowering carcass grade is a major concern in the pig industry, especially in most breeds of obese type pigs. The mechanisms involved in adipogenesis and fat accumulation in pigs remain unclear. Lysine 2-hydroxyisobutyrylation (Khib), is a novel protein post-translational modification (PTM), which play an important role in transcription, energy metabolism and metastasis of cancer cells, but its role in adipogenesis and fat accumulation has not been shown.

Results

In this study, we first analyzed the modification levels of acetylation (Kac), Khib, crotonylation (Kcr) and succinylation (Ksu) of fibro-adipogenic progenitors (FAPs), myogenic precursors (Myo) and mesenchymal stem cells (MSCs) with varied differentiation potential, and found that only Khib modification in FAPs was significantly higher than that in MSCs. Consistently, in parallel with its regulatory enzymes lysine acetyltransferase 5 (KAT5) and histone deacetylase 2 (HDAC2) protein levels, the Khib levels increased quadratically ( P < 0.01) during adipogenic differentiation of FAPs. KAT5 knockdown in FAPs inhibited adipogenic differentiation, while HDAC2 knockdown enhanced adipogenic differentiation. We also demonstrated that Khib modification favored to adipogenic differentiation and fat accumulation by comparing Khib levels in FAPs and backfat tissues both derived from obese-type pigs (Laiwu pigs) and lean-type pigs (Duroc pigs), respectively. Accordingly, the expression patterns of KAT5 and HDAC2 matched well to the degree of backfat accumulation in obese- and lean-type pigs.

Conclusions

From the perspective of protein translational modification, we are the first to reveal the role of Khib in adipogenesis and fat deposition in pigs, and provided new clues for the improvement of fat accumulation and distribution as expected via genetic selection and nutritional strategy in obese-type pigs.

Supplementary Information

The online version contains supplementary material available at 10.1186/s40104-024-01058-9.

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Most cited references 41

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Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.

Kenneth Livak, Thomas D. Schmittgen (2001)

The two most commonly used methods to analyze data from real-time, quantitative PCR experiments are absolute quantification and relative quantification. Absolute quantification determines the input copy number, usually by relating the PCR signal to a standard curve. Relative quantification relates the PCR signal of the target transcript in a treatment group to that of another sample such as an untreated control. The 2(-Delta Delta C(T)) method is a convenient way to analyze the relative changes in gene expression from real-time quantitative PCR experiments. The purpose of this report is to present the derivation, assumptions, and applications of the 2(-Delta Delta C(T)) method. In addition, we present the derivation and applications of two variations of the 2(-Delta Delta C(T)) method that may be useful in the analysis of real-time, quantitative PCR data. Copyright 2001 Elsevier Science (USA).

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Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase.

Robert Zimmermann, Juliane G. Strauss, Guenter Haemmerle … (2004)

Mobilization of fatty acids from triglyceride stores in adipose tissue requires lipolytic enzymes. Dysfunctional lipolysis affects energy homeostasis and may contribute to the pathogenesis of obesity and insulin resistance. Until now, hormone-sensitive lipase (HSL) was the only enzyme known to hydrolyze triglycerides in mammalian adipose tissue. Here, we report that a second enzyme, adipose triglyceride lipase (ATGL), catalyzes the initial step in triglyceride hydrolysis. It is interesting that ATGL contains a "patatin domain" common to plant acyl-hydrolases. ATGL is highly expressed in adipose tissue of mice and humans. It exhibits high substrate specificity for triacylglycerol and is associated with lipid droplets. Inhibition of ATGL markedly decreases total adipose acyl-hydrolase activity. Thus, ATGL and HSL coordinately catabolize stored triglycerides in adipose tissue of mammals.

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Functions and mechanisms of non-histone protein acetylation

Takeo Narita, Brian T. Weinert, Chunaram Choudhary (2018)

Nε-lysine acetylation was discovered more than half a century ago as a post-translational modification of histones and has been extensively studied in the context of transcription regulation. In the past decade, proteomic analyses have revealed that non-histone proteins are frequently acetylated and constitute a major portion of the acetylome in mammalian cells. Indeed, non-histone protein acetylation is involved in key cellular processes relevant to physiology and disease, such as gene transcription, DNA damage repair, cell division, signal transduction, protein folding, autophagy and metabolism. Acetylation affects protein functions through diverse mechanisms, including by regulating protein stability, enzymatic activity, subcellular localization and crosstalk with other post-translational modifications and by controlling protein-protein and protein-DNA interactions. In this Review, we discuss recent progress in our understanding of the scope, functional diversity and mechanisms of non-histone protein acetylation.

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Author and article information

Contributors

Xin Zhang: zhangx0904@cau.edu.cn

Jingdong Yin:

ORCID: http://orcid.org/0000-0003-4623-0568

yinjd@cau.edu.cn

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 (London )

ISSN (Print): 1674-9782

ISSN (Electronic): 2049-1891

Publication date (Electronic): 12 July 2024

Publication date PMC-release: 12 July 2024

Publication date Collection: 2024

Volume: 15

Electronic Location Identifier: 99

Affiliations

[1 ]GRID grid.22935.3f, ISNI 0000 0004 0530 8290, State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, , China Agricultural University, ; Beijing, 100193 China

[2 ]GRID grid.419897.a, ISNI 0000 0004 0369 313X, Molecular Design Breeding Frontier Science Center of the Ministry of Education (MOE), ; Beijing, 100193 China

[3 ]College of Animal Science and Veterinary Medicine, Shandong Agricultural University, ( https://ror.org/02ke8fw32) Taian, 271018 Shandong Province, China

Author information

Jingdong Yin http://orcid.org/0000-0003-4623-0568

Article

Publisher ID: 1058

DOI: 10.1186/s40104-024-01058-9

PMC ID: 11242017

PubMed ID: 38992763

SO-VID: e8a30315-b104-4b14-b6e1-48f2e996166c

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

History

Date received : 6 February 2024

Date accepted : 3 June 2024

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ScienceOpen disciplines: Animal science & Zoology

Keywords: adipogenesis,backfat,fat accumulation,2-hydroxyisobutyrylation,intramuscular fat content,pigs

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ScienceOpen disciplines: Animal science & Zoology

Keywords: adipogenesis, backfat, fat accumulation, 2-hydroxyisobutyrylation, intramuscular fat content, pigs

Lysine 2-hydroxyisobutyrylation levels determined adipogenesis and fat accumulation in adipose tissue in pigs

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Abstract

Background

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Supplementary Information

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Most cited references 41

Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.

Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase.

Functions and mechanisms of non-histone protein acetylation

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