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      Determination of the Heterogeneity of Intramuscular Fat and Visceral Adipose Tissue From Dezhou Donkey by Lipidomics and Transcriptomics Profiling

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          Abstract

          Intramuscular fat (IMF) and visceral adipose tissue (VAT) are both lipids, but have significantly different deposition processes. Furthermore, the heterogeneity of lipid molecular characteristics and mechanisms is unclear. Accordingly, this study used non-targeted lipidomics and transcriptomics to analyze the lipid profiles and metabolism of longissimus dorsi muscle (LDM) and VAT from donkeys. A total of 1,146 and 1,134 lipids belonging to 18 subclasses were identified in LDM and VAT, respectively, with LDM having higher glycerophospholipid (GP) and lower glycerolipid (GL) contents. Polyunsaturated fatty acids (PUFAs) were distributed preferentially at the sn-1 positions in triglycerides (TGs), and sn-2 positions in phosphatidylcholine (PC) and phosphatidylethanolamine (PE). The percentage PUFA content in TGs was significantly lower in LDM than in VAT, while the opposite trend was observed for PUFAs in PC and PE. A total of 110 different lipid molecules (72 downregulated and 38 upregulated) were identified in LDM compared with VAT, of which 11 were considered potential lipid markers. These different lipids were involved in 17 metabolic pathways, including GL and GP metabolisms. Of the 578 differentially expressed genes screened, 311 were downregulated and 267 were upregulated in LDM compared with VAT. Enriched ontology analysis of the differentially expressed genes mainly involved sphingolipid signaling pathways, and GP, GL, and sphingolipid metabolisms. Overall, lipidomics and transcriptomics indicated differences in lipid profiles and metabolism in LDM and VAT, providing new perspectives for the study of heterogeneity in IMF and VAT.

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          Most cited references36

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          Fat deposition, fatty acid composition and meat quality: A review.

          This paper reviews the factors affecting the fatty acid composition of adipose tissue and muscle in pigs, sheep and cattle and shows that a major factor is the total amount of fat. The effects of fatty acid composition on meat quality are also reviewed. Pigs have high levels of polyunsaturated fatty acids (PUFA), including the long chain (C20-22) PUFA in adipose tissue and muscle. The full range of PUFA are also found in sheep adipose tissue and muscle whereas cattle 'conserve' long chain PUFA in muscle phospholipid. Linoleic acid (18:2n-6) is a major ingredient of feeds for all species. Its incorporation into adipose tissue and muscle in relation to the amount in the diet is greater than for other fatty acids. It is deposited in muscle phospholipid at a high level where it and its long chain products eg aracidonic acid (20:4n-6) compete well for insertion into phospholipid molecules. Its proportion in pig adipose tissue declines as fat deposition proceeds and is an index of fatness. The same inverse relationships are not seen in ruminant adipose tissue but in all species the proportion of 18:2n-6 declines in muscle as fat deposition increases. The main reason is that phospholipid, where 18:2n-6 is located, declines as a proportion of muscle lipid and the proportion of neutral lipid, with its higher content of saturated and monounsaturated fatty acids, increases. Oleic acid (18:1cis-9), formed from stearic acid (18:0) by the enzyme stearoyl Co-A desaturase, is a major component of neutral lipid and in ruminants the same enzyme forms conjugated linoleic acid (CLA), an important nutrient in human nutrition. Like 18:2n-6, α-linolenic acid (18:3n-3) is an essential fatty acid and is important to ruminants since it is the major fatty acid in grass. However it does not compete well for insertion into phospholipid compared with 18:2n-6 and its incorporation into adipose tissue and muscle is less efficient. Greater biohydrogenation of 18:3n-3 and a long rumen transit time for forage diets also limits the amount available for tissue uptake compared with 18:2n-6 from concentrate diets. A positive feature of grass feeding is that levels of the nutritionally important long chain n-3 PUFA are increased ie EPA (20:5n-3) and DHA (22:6n-3). Future research should focus on increasing n-3 PUFA proportions in lean carcasses and the use of biodiverse pastures and conservation processes which retain the benefits of fresh leafy grass offer opportunities to achieve this. The varying fatty acid compositions of adipose tissue and muscle have profound effects on meat quality. Fatty acid composition determines the firmness/oiliness of adipose tissue and the oxidative stability of muscle, which in turn affects flavour and muscle colour. Vitamin E is an essential nutrient, which stabilises PUFA and has a central role in meat quality, particularly in ruminants.
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            PPARγ signaling and metabolism: the good, the bad and the future.

            Thiazolidinediones (TZDs) are potent insulin sensitizers that act through the nuclear receptor peroxisome proliferator-activated receptor-γ (PPARγ) and are highly effective oral medications for type 2 diabetes. However, their unique benefits are shadowed by the risk for fluid retention, weight gain, bone loss and congestive heart failure. This raises the question as to whether it is possible to build a safer generation of PPARγ-specific drugs that evoke fewer side effects while preserving insulin-sensitizing potential. Recent studies that have supported the continuing physiologic and therapeutic relevance of the PPARγ pathway also provide opportunities to develop newer classes of molecules that reduce or eliminate adverse effects. This review highlights key advances in understanding PPARγ signaling in energy homeostasis and metabolic disease and also provides new explanations for adverse events linked to TZD-based therapy.
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              How Muscle Structure and Composition Influence Meat and Flesh Quality

              Skeletal muscle consists of several tissues, such as muscle fibers and connective and adipose tissues. This review aims to describe the features of these various muscle components and their relationships with the technological, nutritional, and sensory properties of meat/flesh from different livestock and fish species. Thus, the contractile and metabolic types, size and number of muscle fibers, the content, composition and distribution of the connective tissue, and the content and lipid composition of intramuscular fat play a role in the determination of meat/flesh appearance, color, tenderness, juiciness, flavor, and technological value. Interestingly, the biochemical and structural characteristics of muscle fibers, intramuscular connective tissue, and intramuscular fat appear to play independent role, which suggests that the properties of these various muscle components can be independently modulated by genetics or environmental factors to achieve production efficiency and improve meat/flesh quality.
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                Author and article information

                Contributors
                Journal
                Front Nutr
                Front Nutr
                Front. Nutr.
                Frontiers in Nutrition
                Frontiers Media S.A.
                2296-861X
                28 September 2021
                2021
                : 8
                : 746684
                Affiliations
                Liaocheng Research Institute of Donkey High-Efficiency Breeding and Ecological Feeding, College of Agronomy, Liaocheng University , Liaocheng, China
                Author notes

                Edited by: Zhaojun Wei, Hefei University of Technology, China

                Reviewed by: Jun Wang, Hefei University, China; Fan Zhang, Hefei University of Technology, China; Ningyang Li, Shandong Agricultural University, China

                *Correspondence: Changfa Wang wangcf1967@ 123456163.com

                This article was submitted to Nutrition and Food Science Technology, a section of the journal Frontiers in Nutrition

                †ORCID: Mengmeng Li orcid.org/0000-0002-6317-875X

                Article
                10.3389/fnut.2021.746684
                8505748
                34651009
                91bf987f-9e87-45d4-aa6e-d70df4a0fb3d
                Copyright © 2021 Li, Zhu, Chai, Wang, Song, Liu, Cai, Song, Sun, Xue and Wang.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 July 2021
                : 01 September 2021
                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 36, Pages: 11, Words: 6069
                Categories
                Nutrition
                Original Research

                dezhou donkey,lipidomics,transcriptomics,heterogeneity,intramuscular fat,visceral adipose tissue

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