The impact of protein quantity during energy restriction on genome-wide gene expression in adipose tissue of obese humans

Bussel, I.P.G. van; Backx, Evelien; Groot, Lisette C. P. G. M. de; Tieland, Michael; Müller, Michael; Afman, Lydia A.

doi:10.1038/ijo.2017.76

Cited by 4 publications

(5 citation statements)

References 34 publications

(23 reference statements)

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“…An 8-wk trial of an energy-restricted high (30% energy) compared with a low (15% energy) protein diet indicated that high compared with low protein, and meat protein in particular, but not plant or fish protein, increased a score that included CRP, IL-6, TNF-α, and PAI-1 concentrations (27). Another 12-wk trial of protein intake in the context of 10% energy restriction, this one in overweight, older participants, indicated that a high-protein diet (1.7 g · kg body weight –1 · d –1 ) compared to a normal-protein diet (0.9 g · kg body weight –1 · d –1 ) induced differential expression in 530 genes in white adipose tissue, notably a downregulation in expression of genes linked to immune cell infiltration, adaptive immune response and inflammasome in the normal-protein group, but not the high-protein group (46). However, a 6-wk ad libitum high animal compared with high plant protein (30% energy) diet in overweight or obese individuals with nonalcoholic fatty liver disease and type 2 diabetes showed no differences in IL-6 or MCP-1 between diets, a decrease in IL-18 only in the high animal protein group, and a decrease in TNF-α only in the plant protein group (24).…”

Section: Discussionmentioning

confidence: 99%

Dietary Protein and Changes in Biomarkers of Inflammation and Oxidative Stress in the Framingham Heart Study Offspring Cohort

Hruby¹,

Jacques²

2019

Current Developments in Nutrition

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Background Chronic inflammation is thought to be a major characteristic of aging, which may increase need for substrates, specifically protein, to support anti-inflammatory processes. Objectives The aim of this study was to assess associations between dietary protein and changes in biomarkers of inflammation and oxidative stress over the long term in a community-dwelling population. Methods In 2061 participants of the Framingham Heart Study Offspring cohort who attended exams 7 (1998–2001; mean ± SD age 60.0 ± 8.8 y, 56% female) and 8 (2005–2008), total, animal, and plant protein intakes were assessed by food-frequency questionnaire at each exam, energy adjusted, and averaged. We defined an inflammation and oxidative stress score as the sum of rank-normalized values of 9 circulating biomarkers (C-reactive protein, osteoprotegerin, P-selectin, tumor necrosis factor receptor II, soluble intercellular adhesion molecule-1, interleukin 6, monocyte chemoattractant protein 1, and lipoprotein phospholipase A2 mass and activity), and urinary isoprostanes, along with 2 subscores. Adjusted least-square means of changes in the scores and log individual biomarkers in quartile categories of intake were estimated with the use of linear regression models, across mean ± SD 6.6 ± 0.7 y of follow-up. Results Protein intake was inversely associated with changes in the inflammation and oxidative stress score (mean ± SE in Q1 compared with Q4: 0.77 ± 0.17 compared with 0.31 ± 0.19; P -trend = 0.02), indicating overall inflammation/oxidative stress increased less in those with the highest intake than in those with the lowest. Favorable associations were observed for plant protein (Q1 compared with Q4: 0.89 ± 0.25 compared with 0.14 ± 0.25; P -trend = 0.001), but only trended toward significance for animal protein (Q1 compared with Q4: 0.70 ± 0.26 compared with 0.31 ± 0.26; P -trend = 0.05). Total protein and plant protein intakes were also inversely associated with changes in monocyte chemoattractant protein 1 (total: Q1 compared with Q4: 0.19 ± 0.01 compared with 0.15 ± 0.01 log-pg/mL; P -trend = 0.03; plant: Q1 compared with Q4: 0.21 ± 0.01 compared with 0.16 ± 0.01 log-pg/mL; P -trend = 0.003). Conclusions Dietary protein, particularly from plant sources, may be associated with beneficial changes in the inflammatory burden in aging populations.

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Section: Discussionmentioning

confidence: 99%

Dietary Protein and Changes in Biomarkers of Inflammation and Oxidative Stress in the Framingham Heart Study Offspring Cohort

Hruby¹,

Jacques²

2019

Current Developments in Nutrition

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“…Furthermore, a genome-wide association study [ 72 ] explored the effects of protein quantity in diets during energy restriction on OR gene expression in white adipose tissue (WAT). This study revealed that high-protein energy restriction (HP-ER) diets resulted in distinct gene expression changes compared to normal-protein energy restriction (NP-ER) diets.…”

Section: Resultsmentioning

confidence: 99%

“…Additionally, patients with a higher BMI also showed improvements in odor identification tasks upon intranasal insulin administration [ 86 ]. Another study indicated that the presence of insulin in the olfactory bulb could be connected with the process of satiation and the pathogenesis of obesity [ 72 ]. GLP-1 agonist treatment decreases the olfactory preference for sweet- and fat-enriched food [ 87 ] and improves olfactory sensitivity and odor-induced right parahippocampal activation [ 88 ].…”

Section: Resultsmentioning

confidence: 99%

The Role of the Olfactory System in Obesity and Metabolism in Humans: A Systematic Review and Meta-Analysis

Matiashova,

Hoogkamer,

Timper

2023

Metabolites

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Obesity, linked to chronic diseases, poses a global health challenge. While the role of the olfactory system in energy homeostasis is well-documented in rodents, its role in metabolism regulation and obesity in humans remains understudied. This review examines the interplay between olfactory function and metabolic alterations in human obesity and the effects of bariatric surgery on olfactory capabilities in humans. Adhering to PRISMA guidelines, a systematic review and meta-analysis was conducted, focusing exclusively on original human studies. From 51 articles, 14 were selected for the meta-analysis. It was found that variations in olfactory receptor genes influence the susceptibility to odors and predisposition to weight gain and poor eating habits. Bariatric surgery, particularly sleeve gastrectomy, shows significant improvements in olfactory function (SMD 2.37, 95% CI [0.96, 3.77], I = 92%, p = 0.001), especially regarding the olfactory threshold (SMD −1.65, 95% CI [−3.03, −0.27], I = 81%, p = 0.02). There is a bidirectional relationship between olfactory function and metabolism in humans. Bariatric surgery improves olfactory perception in obese patients, but it is still unclear if impacting the olfactory system directly affects eating behavior and the energy balance. However, these findings open novel avenues for future studies addressing the olfactory system as a novel target to alter systemic metabolism in humans.

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“…Additionally, the molecular basis of the individual response to interventions is still poorly understood. For instance, dietary or physical exercise interventions have shown changes in the metabolome (van Dijk et al, 2012; Pellis et al, 2012; Zeevi et al, 2015) but are frequently unable to identify changes in the transcriptome (Van Bussel et al, 2017; Fazelzadeh et al, 2018; ten Haaf et al, 2018). Also, the time-scale needed to investigate responses to interventions remains largely unknown.…”

Section: Introductionmentioning

confidence: 99%

“…These metabolic and caloric challenge tests are regarded upon as novel potential biomarkers of health (van Ommen et al, 2014; Stroeve et al, 2015) recording the phenotypic flexibility of individuals within minutes to hours of the test triggering acute and complex stress responses (energy fluxes, oxidative and inflammatory stress, apoptosis etc.). Hence, there is a need to monitor the response not only by traditional health markers but also at the molecular level (Van Bussel et al, 2017; Catoire et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

A combined lifestyle intervention induces a sensitization of the blood transcriptomic response to a nutrient challenge

Gehrmann

Beekman

Deelen

et al. 2021

Preprint

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The global population is growing older. As age is a primary risk factor of (multi)morbidity, there is a need for novel indicators to predict, track, treat and prevent the development of disease. Lifestyle interventions have shown promising results in improving the health of participants and reducing the risk for disease, but in the elderly population, such interventions often show less reliable or subtle effects on health outcomes. This is further complicated by a poor understanding of the homeodynamics and the molecular effects of lifestyle interventions, by which their effects of a lifestyle intervention remain obscured. In the Growing Old Together (GOTO) study, we examined the responses of 164 healthy, elderly men and women to a 13-week combined physical and dietary lifestyle intervention. In addition to collecting blood samples at a fasted state, we sampled blood also 30 minutes following a standardized meal. This allows us to investigate an intervention response not only in the traditional fasted state, but also in the blood metabolic and cellular responses to a nutrient challenge. We investigated the transcriptomic and metabolomic responses to this nutrient challenge, how these responses relate to each other, and how this response is affected by the lifestyle intervention. We find that the intervention has very little effect on the fasted blood transcriptome, but that the nutrient challenge induces a large translational inhibition, and an innate immune activation, which together comprise a cellular stress response that is stimulated by the intervention. A sex-specific analysis reveals that although the same set of genes respond in the same direction in both males and females, the magnitude of these effects differ, and are modulated differently by the intervention. On the other hand, the metabolomic response to the nutrient challenge is largely unaffected by the intervention, and the correlation between the metabolomic nutrient response and transcriptomic modules indicates that the change in transcriptomic response to the nutrient challenge is independent from a change in cellular metabolomic environment. This work constitutes a glance at the acute transcriptomic stress response to nutrient intake in blood, and how a lifestyle intervention affects this response in healthy elderly, and may lead to the development of novel biomarkers to capture the phenotypic flexibility of health.

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The impact of protein quantity during energy restriction on genome-wide gene expression in adipose tissue of obese humans

Abstract: Based on gene expression changes, we concluded that consumption of normal protein quantity compared with high-protein quantity during ER has a more beneficial effect on inflammation-related gene expression in WAT.

Cited by 4 publications

References 34 publications

Dietary Protein and Changes in Biomarkers of Inflammation and Oxidative Stress in the Framingham Heart Study Offspring Cohort

Dietary Protein and Changes in Biomarkers of Inflammation and Oxidative Stress in the Framingham Heart Study Offspring Cohort

The Role of the Olfactory System in Obesity and Metabolism in Humans: A Systematic Review and Meta-Analysis

A combined lifestyle intervention induces a sensitization of the blood transcriptomic response to a nutrient challenge

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