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Differential effects of bariatric surgery and caloric restriction on hepatic one-carbon and fatty acid metabolism.

ABSTRACT: Weight loss interventions, including dietary changes, pharmacotherapy, or bariatric surgery, prevent many of the adverse consequences of obesity, and may also confer intervention-specific benefits beyond those seen with decreased weight alone. We compared the molecular effects of different interventions on liver metabolism to understand the mechanisms underlying these benefits. Male rats on a high-fat, high-sucrose diet underwent sleeve gastrectomy (SG) or intermittent fasting with caloric restriction (IF-CR), achieving equivalent weight loss. The interventions were compared to ad-libitum (AL)-fed controls. Analysis of liver and blood metabolome and transcriptome revealed distinct and sometimes contrasting metabolic effects between the two interventions. SG primarily influenced one-carbon metabolic pathways, whereas IF-CR increased de novo lipogenesis and glycogen storage. These findings suggest that the unique metabolic pathways affected by SG and IF-CR contribute to their distinct clinical benefits, with bariatric surgery potentially influencing long-lasting changes through its effect on one-carbon metabolism.

SUBMITTER: Haran A

PROVIDER: S-EPMC10300224 | biostudies-literature | 2023 Jul

REPOSITORIES: biostudies-literature

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Differential effects of bariatric surgery and caloric restriction on hepatic one-carbon and fatty acid metabolism.

Haran Arnon A Bergel Michael M Kleiman Doron D Hefetz Liron L Israeli Hadar H Weksler-Zangen Sarah S Agranovich Bella B Abramovich Ifat I Ben-Haroush Schyr Rachel R Gottlieb Eyal E Ben-Zvi Danny D

iScience 20230607 7

Weight loss interventions, including dietary changes, pharmacotherapy, or bariatric surgery, prevent many of the adverse consequences of obesity, and may also confer intervention-specific benefits beyond those seen with decreased weight alone. We compared the molecular effects of different interventions on liver metabolism to understand the mechanisms underlying these benefits. Male rats on a high-fat, high-sucrose diet underwent sleeve gastrectomy (SG) or intermittent fasting with caloric restr ...[more]

PMID: 37389181

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Project description:Purpose: To gain additional insights to candidate factors promoting longevity in Caloric Restricted Conditioned Media (CRCM), we performed transcriptomics analysis (RNA-seq) on BY4741 yeast cells grown in non-restricted SC media supplemented with CRCM, Non-restricted Conditioned Media (NRCM), or water as a control with a goal of identifying physiological responses that could be linked to specific metabolites. Methods: RNA profiles of NR (SC, 2% glucose) treated cells supplemented with water, 2% CRCM, or 2% NRCM at log phase, 24, and 96 hours post-inoculation. These samples were conducted in triplicate. Following inoculation, we harvested cells at log phase, 24 hrs (late diauxic shift), and 96 hrs (stationary phase).Total RNA was isolated using the hot acid phenol method and then processed into Illumina DNA sequencing libraries. Briefly, total RNA was treated with DNase I for 10 min at 37°C and then measured for concentration and quality with an Agilent Bioanalyzer. PolyA mRNA selection was performed on 5µg of the DNase-treated total RNA with the NEBNext Poly(A) mRNA magnetic isolation module (E7490). DNA sequencing libraries were then generated with the NEBNExt Ultra Directional RNA library Prep kit for Illumina (E7420). Libraries were sequenced on an Illumina NextSeq 500 by the UVA Genome Analysis and Technology Core. Results: Sequencing reads were mapped to the sacCer3 genome using bowtie2 with default settings. We preprocessed sequencing data from the UVA genomics core and analyzed differential gene expression in R using DESeq2. We found that In log phase cells, there were no significantly upregulated or downregulated genes in the CRCM or NRCM samples as compared to the water supplemented control (FDR <0.05). At the 24 hr timepoint, CRCM samples diverged from the NRCM and water supplemented control samples, and showed many more differentially regulated genes than the NRCM-treated samples. At the 96 hr timepoint, NRCM samples also became more clearly separated from the control in a PCA plot , though there were still a large number of genes exclusively altered in the CRCM samples. Furthermore, the YCL064C (CHA1) gene clearly stood out as being the most significantly upregulated in conditioned media supplementation. Conclusions: RNAseq data led us to explore YCL064C (CHA1) gene clearly stood out as being the most significantly upregulated in the conditioned media experiments. CHA1 encodes a predominantly mitochondrial L-serine (L-threonine) deaminase that catabolizes these amino acids. RNA-seq based transcriptome analysis allowed us to explore L-serine contribution to longevity phenotype we observed with CRCM.

Project description:BackgroundEmbryonic and fetal development is very susceptible to the availability of nutrients that can interfere with the setting of epigenomes, thus modifying the main metabolic pathways and impacting the health and phenotypes of the future individual. We have previously reported that a 38% reduction of the methyl donor methionine in the diet of 30 female ducks reduced the body weight of their 180 mule ducklings compared to that of 190 ducklings from 30 control females. The maternal methionine-restricted diet also altered plasmatic parameters in 30 of their ducklings when compared to that of 30 ducklings from the control group. Thus, their plasma glucose and triglyceride concentrations were higher while their free fatty acid level and alanine transaminase activity were decreased. Moreover, the hepatic transcript level of 16 genes involved in pathways related to energy metabolism was significantly different between the two groups of ducklings. In the present work, we continued studying the liver of these newly hatched ducklings to explore the impact of the maternal dietary methionine restriction on the hepatic transcript level of 70 genes mostly involved in one-carbon metabolism and epigenetic mechanisms.ResultsAmong the 12 genes (SHMT1, GART, ATIC, FTCD, MSRA, CBS, CTH, AHCYL1, HSBP1, DNMT3, HDAC9 and EZH2) identified as differentially expressed between the two maternal diet groups (p-value < 0.05), 3 of them were involved in epigenetic mechanisms. Ten other studied genes (MTR, GLRX, MTHFR, AHCY, ADK, PRDM2, EEF1A1, ESR1, PLAGL1, and WNT11) tended to be differently expressed (0.05 < p-value < 0.10). Moreover, the maternal dietary methionine restriction altered the number and nature of correlations between expression levels of differential genes for one-carbon metabolism and epigenetic mechanisms, expression levels of differential genes for energy metabolism, and phenotypic traits of ducklings.ConclusionThis avian model showed that the maternal dietary methionine restriction impacted both the mRNA abundance of 22 genes involved in one-carbon metabolism or epigenetic mechanisms and the mRNA abundance of 16 genes involved in energy metabolism in the liver of the newly hatched offspring, in line with the previously observed changes in their phenotypic traits.

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Differential effects of bariatric surgery and caloric restriction on hepatic one-carbon and fatty acid metabolism.

Publications

Differential effects of bariatric surgery and caloric restriction on hepatic one-carbon and fatty acid metabolism.

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