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Metabolomics of heat stress response in pig adipose tissue reveals alteration of phospholipid and fatty acid composition during heat stress.

ABSTRACT: To determine the effect of heat stress (HS) on adipose tissue metabolome, a combination of liquid chromatography-mass spectrometry-based metabolomics profiling approaches was applied to characterize changes of metabolite classes in adipocytes differentiated in culture (in vitro) and mesenteric adipose tissue of pigs exposed to HS (in vivo). Effect of HS on the composition of individual fatty acids in cultured adipocytes, mesenteric adipose tissue, and serum of animals was also investigated using gas chromatography analysis. In vitro, preadipocytes were differentiated either under control (37 °C) or HS (41.5 °C) temperature for 9 d. For the animal experiment, pigs were kept either in control (Con) environment (20 °C) with ad libitum feed intake, HS (35 °C) temperature with ad libitum feed intake (HS), or at 20 °C with pair feeding to the HS pigs. In cultured cells, HS increased triglyceride and decreased monoacylglycerol (P < 0.05) species accumulation compared with control. Phosphatidylinositol and phosphatidylserine were increased by HS, whereas phosphatidylcholine, phosphatidylethanolamine, and phosphatidylglycerol were decreased relative to control (P < 0.05). Heat-stressed adipocytes in culture also had higher concentrations of saturated (SFA) and monounsaturated fatty acids (P < 0.05) relative to control. Pathways of proline and biotin metabolism were elevated (P < 0.05) by HS in adipocytes. The metabolomics signatures in adipocytes cultured under HS indicates that pathways centered around diacylglycerol metabolism are impacted by HS. In adipose tissue from animals in the HS treatment, there was increased (P < 0.05) abundance of 4,8 dimethylnonanoyl carnitine (P < 0.05). Heat-stressed animals also had higher (P < 005) serum linoleic, total polyunsaturated fatty acids, and decreased total SFA than PF (P < 0.05). These results indicate that HS elevates lipogenic pathways while suppressing fatty acid oxidation and demonstrate the usefulness of metabolomics analysis as a tool for determining the impact of HS in pig tissues.

SUBMITTER: Qu H

PROVIDER: S-EPMC6095270 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Metabolomics of heat stress response in pig adipose tissue reveals alteration of phospholipid and fatty acid composition during heat stress.

Qu Huan H Ajuwon Kolapo M KM

Journal of animal science 20180701 8

To determine the effect of heat stress (HS) on adipose tissue metabolome, a combination of liquid chromatography-mass spectrometry-based metabolomics profiling approaches was applied to characterize changes of metabolite classes in adipocytes differentiated in culture (in vitro) and mesenteric adipose tissue of pigs exposed to HS (in vivo). Effect of HS on the composition of individual fatty acids in cultured adipocytes, mesenteric adipose tissue, and serum of animals was also investigated using ...[more]

PMID: 29961875

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Project description:Heat stress (HS) negatively impacts several swine production variables, including carcass fat quality and quantity. Pigs reared in HS have more adipose tissue than energetically predicted, explainable, in part, by HS-induced hyperinsulinemia. Study objectives were to evaluate insulin's role in altering fat characteristics during HS via feeding insulin-sensitizing compounds. Forty crossbred barrows (113 ± 9 kg BW) were randomly assigned to one of five environment by diet treatments: 1) thermoneutral (TN) fed ad libitum (TNAL), 2) TN and pair-fed (TNPF), 3) HS fed ad libitum (HSAL), 4) HS fed ad libitum with sterculic oil (SO) supplementation (HSSO; 13 g/d), and 5) HS fed ad libitum with dietary chromium (Cr) supplementation (HSCr; 0.5 mg/d; Kemin Industries, Des Moines, IA). The study consisted of three experimental periods (P). During P0 (2 d), all pigs were exposed to TN conditions (23 ± 3 °C, 68 ± 10% RH) and fed ad libitum. During P1 (7 d), all pigs received their respective dietary supplements, were maintained in TN conditions, and fed ad libitum. During P2 (21 d), HSAL, HSSO, and HSCr pigs were fed ad libitum and exposed to cyclical HS conditions (28 to 33 °C, 58 ± 10% RH). The TNAL and TNPF pigs remained in TN conditions and were fed ad libitum or pair-fed to their HSAL counterparts. Rectal temperature (TR), respiration rate (RR), and skin temperature (TS) were obtained daily at 0600 and 1800 h. At 1800 h, HS exposed pigs had increased TR, RR, and TS relative to TNAL controls (1.13 °C, 48 bpm, and 3.51 °C, respectively; P < 0.01). During wk 2 and 3 of P2, HSSO pigs had increased 1800 h TR relative to HSAL and HSCr (~0.40 and ~0.42 °C, respectively; P ≤ 0.05). Heat stress decreased ADFI and ADG compared to TNAL pigs (2.24 vs. 3.28 and 0.63 vs. 1.09 kg/d, respectively; P < 0.01) and neither variable was affected by SO or Cr supplementation. Heat stress increased or tended to increase moisture content of abdominal (7.7 vs. 5.9%; P = 0.07) and inner s.c. (11.4 vs. 9.8%; P < 0.05) adipose depots compared to TNAL controls. Interestingly, TNPF pigs also had increased adipose tissue moisture content and this was most pronounced in the outer s.c. depot (15.0 vs. 12.2%; P < 0.01) compared to TNAL pigs. Heat stress had little or no effect on fatty acid composition of abdominal, inner, and outer s.c. adipose tissue depots. In summary, the negative effects of HS on fat quality do not appear to be fatty acid composition related, but may be explained by increased adipose tissue moisture content.

Project description:IGF2:g.3072G>A polymorphism has been described as the causal mutation of a maternally imprinted QTL for muscle growth and fat deposition in pigs. The objective of the current work was to study the association between the IGF2:g.3072G>A polymorphism and the IGF2 gene expression and its effect on fatty acid composition in adipose tissue in different pig genetic backgrounds. A cis-eQTL region associated with the IGF2 mRNA expression in adipose tissue was identified in an eGWAS with 355 animals. The IGF2 gene was located in this genomic interval and IGF2g.3072G>A was the most significant SNP, explaining a 25% of the gene expression variance. Significant associations between IGF2:g.3072G>A polymorphism and oleic (C18:1(n-9); p-value = 4.18x10-07), hexadecanoic (C16:1(n-9); p-value = 4.04x10-07), linoleic (C18:2(n-6); p-value = 6.44x10-09), α-linoleic (C18:3(n-3); p-value = 3.30x10-06), arachidonic (C20:4(n-6); p-value = 9.82x10-08) FAs and the MUFA/PUFA ratio (p-value = 2.51x10-9) measured in backfat were identified. Animals carrying the A allele showed an increase in IGF2 gene expression and higher PUFA and lower MUFA content. However, in additional studies was observed that there could be other proximal genetic variants affecting FA composition in adipose tissue. Finally, no differences in the IGF2 gene expression in adipose tissue were found between heterozygous animals classified according to the IGF2:g.3072G>A allele inherited from the father (APGM or AMGP). However, pyrosequencing analysis revealed that there is imprinting of the IGF2 gene in muscle and adipose tissues, with stronger differences among the paternally and maternally inherited alleles in muscle. Our results suggested that IGF2:g.3072G>A polymorphism plays an important role in the regulation of IGF2 gene expression and can be involved in the fatty acid composition in adipose tissue. In both cases, further studies are still needed to deepen the mechanism of regulation of IGF2 gene expression in adipose tissue and the IGF2 role in FA composition.

Dataset Information

Metabolomics of heat stress response in pig adipose tissue reveals alteration of phospholipid and fatty acid composition during heat stress.

Publications

Metabolomics of heat stress response in pig adipose tissue reveals alteration of phospholipid and fatty acid composition during heat stress.

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