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A saturated fatty acid–rich diet induces an obesity-linked proinflammatory gene expression profile in adipose tissue of subjects at risk of metabolic syndrome
Open accessAbstract
Background Changes in dietary fat composition could lower the risk of developing metabolic syndrome. Adipose tissue is an interesting tissue in this respect because of its role in lipid metabolism and inflammation.Objective Our objective was to investigate the effect of a saturated fatty acid (SFA)- and a monounsaturated fatty acid (MUFA)-rich diet on insulin sensitivity, serum lipids, and gene expression profiles of adipose tissue in subjects at risk of metabolic syndrome.Design A parallel controlled-feeding trial was conducted in 20 abdominally overweight subjects. Subjects received an SFA diet or a MUFA diet for 8 wk. Plasma and subcutaneous adipose tissue samples were obtained, and insulin sensitivity was measured by using a hyperinsulinemic-euglycemic clamp. Adipose tissue samples underwent whole-genome microarray and histologic analysis. Plasma and adipose tissue fatty acid composition and concentrations of serum cholesterol and plasma cytokine were determined.Results Consumption of the SFA diet resulted in increased expression of genes involved in inflammation processes in adipose tissue, without changes in morphology or insulin sensitivity. The MUFA diet led to a more antiinflammatory gene expression profile, which was accompanied by a decrease in serum LDL-cholesterol concentrations and an increase in plasma and adipose tissue oleic acid content.Conclusions Consumption of an SFA diet resulted in a proinflammatory "obesity-linked" gene expression profile, whereas consumption of a MUFA diet caused a more antiinflammatory profile. This suggests that replacement of dietary SFA with MUFA could prevent adipose tissue inflammation and may reduce the risk of inflammation-related diseases such as metabolic syndrome. This trial was registered at clinicaltrials.gov as NCT00405197.
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“especially considering that the impact of fatty acids on metabolic health is dictated by their chemical characteristics with unsaturated fatty acids, medium- and short-chain fatty acids being proven as beneficial to metabolic health, compared to long-chain saturated fatty acids (Roche, 2005; Holland et al., 2007; van Dijk et al., 2009;”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as van Dijk et al., 2009
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“The inclusion of refined olive oil to provide 20% of their intake as monounsaturated fatty acids compared to the 11% of the saturated diet led to a more anti-inflammatory gene expression profile [20].”
Backgroundvan der Velpen, V., Geelen, A., Hollman, P. C. H., Schouten, E. G., Veer, P. V. ’., & Afman, L. A. (2014) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.088484 · Cited by 46
Nutritional Health Considerations for Persons with Spinal Cord Injury
Bigford, G. E., & Nash, M. S. (2017) · Topics in Spinal Cord Injury Rehabilitation · doi:10.1310/sci2303-188 · Cited by 50
Michielsen, C. C. J. R., Hangelbroek, R., Feskens, E. J. M., & Afman, L. A. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201801095 · Cited by 48
Berg, J., Seyedsadjadi, N., & Grant, R. (2020) · International Journal of Tryptophan Research · doi:10.1177/1178646920981946 · Cited by 44
Kim, N., Lee, J. O., Lee, H. J., Kim, H. I., Kim, J. K., Lee, S. K., Lee, S. K., Kim, S. J., Park, S. H., & Kim, H. S. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.657379 · Cited by 46
“Some studies indicate that saturated FAs induce obesity and diabetes (19), whereas long chain polyunsaturated omega-3 FAs protect against these diseases.”
BackgroundGuerendiain, M., Montes, R., López‐Belmonte, G., Martín‐Matillas, M., Castellote, A. I., Martín-Bautista, E., Martí, A., Martínez, J. A., Moreno, L. A., Garagorri, J. M., et al. (2016) · Clinical Nutrition · doi:10.1016/j.clnu.2016.11.006 · Cited by 44
Moustafa, J. S. E.-S., Eleftherohorinou, H., de Smith, A. J., Andersson‐Assarsson, J. C., Alves, A. C., Hadjigeorgiou, E., Walters, R. G., Asher, J. E., Bottolo, L., Buxton, J. L., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds187 · Cited by 47
“Gene expression analysis from subcutaneous adipose tissue of moderately overweight individuals (n 1⁄4 20) at risk of metabolic syndrome subjected to a 2-week run-in saturated fat diet followed by a 8-week diet intervention was obtained from gene expression omnibus data set GDS3678 (32).”
MethodInfluentialCorella, D., & Ordovás, J. M. (2014) · BioEssays · doi:10.1002/bies.201300180 · Cited by 45
“Hence, a high-SFA diet [59] increased the expression of genes involved in inflammation processes in adipose tissue, whereas a high-MUFA diet led to a more anti-inflammatory gene expression profile.”
BackgroundZhao, M., Zang, B., Cheng, M., Ma, Y., Yang, Y.-H., & Yang, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078620 · Cited by 42
“High-fat diets, especially high-fat diet enriched with saturated fatty acid exert more deleterious effect on insulin sensitivity and inflammation response [13,52,53].”
BackgroundHannon, B. A., Thompson, S. V., An, R., & Terán-García, M. (2017) · Annals of Nutrition and Metabolism · doi:10.1159/000477216 · Cited by 43
Cicco, P. D., Maisto, M., Tenore, G. C., & Ianaro, A. (2020) · Nutrients · doi:10.3390/nu12123663 · Cited by 44
Pros and cons of fatty acids in bone biology
Wauquier, F., Léotoing, L., Philippe, C., Spilmont, M., Coxam, V., & Wittrant, Y. (2015) · Progress in Lipid Research · doi:10.1016/j.plipres.2015.03.001 · Cited by 41
Dietary Macronutrient and Energy Intake and Urinary Incontinence in Women
Maserejian, N. N., Giovannucci, E. L., McVary, K. T., McGrother, C. W., & McKinlay, J. B. (2010) · American Journal of Epidemiology · doi:10.1093/aje/kwq065 · Cited by 41
“The possibility that an effect of total energy intake is stronger in leaner women is plausible, in that leaner women may have fewer competing causes of urinary incontinence than overweight women, whose urinary incontinence may be more likely to be related to intraabdominal pressure (13) or effects of the proinflammato…”
BackgroundLuque‐Sierra, A., Álvarez‐Amor, L., Kleemann, R., Martı́n, F., & Varela, L. M. (2018) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201800295 · Cited by 42
Ströher, D. J., de Oliveira, M. F., Oliveira, P. M., Pilar, B. C., Cattelan, M. D. P., Rodrigues, E., Bertolin, K., Gonçalves, P. B. D., Piccoli, J. D. C. E., & Manfredini, V. (2019) · Journal of Medicinal Food · doi:10.1089/jmf.2019.0172 · Cited by 43
“A high SFA intake has been associated with proinflammatory response and gene regulation involved in inflammatory pathways, such as TNF-a, in adipose tissue.(59,60) In contrast, we observed a reduction in the amount of adiponectin messenger RNA (mRNA) expression, with increasing adipocyte size when VCO was combined wit…”
BackgroundNeuhouser, M. L., Howard, B. V., Lu, J., Tinker, L. F., Horn, L. V., Caan, B. J., Rohan, T. E., Stefanick, M. L., & Thomson, C. A. (2012) · Metabolism · doi:10.1016/j.metabol.2012.04.007 · Cited by 40
Polari, L., Yatkin, E., Martínez Chacón, M. G., Ahotupa, M., Smeds, A., Strauss, L., Zhang, F., Poutanen, M., Saarinen, N., & Mäkelä, S. I. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.06.002 · Cited by 38
Colvin, B. N., Longtine, M. S., Chen, B., Costa, M. L., & Nelson, D. M. (2017) · Reproduction · doi:10.1530/rep-16-0576 · Cited by 37
Nutritional Properties of Quinoa
Wu, G. (2015) · Wiley eBooks · doi:10.1002/9781118628041.ch11 · Cited by 37
Vaittinen, M., Männistö, V., Käkelä, P., Ågren, J., Tiainen, M., Schwab, U., & Pihlajamäki, J. (2017) · Obesity · doi:10.1002/oby.21753 · Cited by 36
“(13), who showed that an SFA-rich diet increased, and an MUFArich diet reduced, the expression of inflammatory genes in AT.”
BackgroundUrpí-Sardà, M., Casas, R. M., Sacanella, E., Corella, D., Andrés‐Lacueva, C., Llorach, R., Garrabou, G., Cardellach, F., Sala‐Vila, A., Ros, E., et al. (2021) · Biomedicines · doi:10.3390/biomedicines9080862 · Cited by 35
“Other intervention studies with diets rich in SFA and MUFA have shown similar results with decreases in RANTES expression with these two diets [35].”
ResultA practical approach to the metabolic syndrome: review of current concepts and management
Tota-Maharaj, R., DeFilippis, A. P., Blumenthal, R. S., & Blaha, M. J. (2010) · Current Opinion in Cardiology · doi:10.1097/hco.0b013e32833cd474 · Cited by 35
Mechanism of Obesity-Related Lipotoxicity and Clinical Perspective
Engin, A. B. (2024) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-63657-8_5 · Cited by 37
Alemany, M. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.03.003 · Cited by 36
“, within physiological limits) produce functional and regulatory damages in the tissue [16,17].”
BackgroundThe Regulation of Lipokines by Environmental Factors
Hernández‐Saavedra, D., & Stanford, K. I. (2019) · Nutrients · doi:10.3390/nu11102422 · Cited by 34
“MUFAs play an important role in stress and inflammation [72–75], and the consumption of a MUFA-rich diet in overweight subjects reduces the pro-inflammatory profile and, thus, leads to risk reduction for metabolic diseases [76].”
BackgroundBiomarkers of Nutrient Bioactivity and Efficacy
Rubio‐Aliaga, I., Kochhar, S., & Silva‐Zolezzi, I. (2012) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e3182548df2 · Cited by 34
Individualized Weight Management: What Can Be Learned from Nutrigenomics and Nutrigenetics?
Rudkowska, I., & Përusse, L. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-398397-8.00014-9 · Cited by 34
“A study by van Dijk et al.(18) demonstrated that consumption of an SFA-rich diet resulted in increased expression of genes involved in inflammation processes.”
BackgroundInfluentialÓvilo, C., Benítez, R., Fernández, A. I., Isabel, B., Núñez, Y., Fernández, A. I., Rodríguez, C., Daza, A., Silio, L. F., & López-Bote, C. J. (2014) · Journal of Animal Science · doi:10.2527/jas.2013-6988 · Cited by 34
“…that characterize the Iberian pig breed used here support that animals fed the CH diet could be starting to develop some early signals of obesity, as gene expression changes in proinflammatory genes are observed before adipose tissue morphology is phenotypically affected (Van Dijk et al., 2009).”
BackgroundDordevic, A. L., Konstantopoulos, N., & Cameron‐Smith, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099382 · Cited by 32
The Prevalence of Metabolic Syndrome and Its Related Risk Complications among Koreans
Lee, S.-H., Tao, S., & Kim, H. (2019) · Nutrients · doi:10.3390/nu11081755 · Cited by 32
“To sum up, the prevalence of MetS was not significantly associated with the geographical location of participants, while the social and cultural facets of the respondents more affected the prevalence of MetS [9,27].”
BackgroundResult
Metadata
- Authors
- van Dijk, S. J., Feskens, E. J., Bos, M. B., Hoelen, D. W., Heijligenberg, R., Bromhaar, M. G., de Groot, L. C., de Vries, J. H., Müller, M., & Afman, L. A.
- Affiliations
- TiFN (NL)
- Corresponding author
- Afman, Lydia A
- Venue
- The American Journal of Clinical Nutrition
- Publisher
- Elsevier BV
- Published
- 2009-12
- Volume
- 90
- Issue
- 6
- Pages
- 1656-1664
- ISSN
- 0002-9165 (ISSN-L)
- OpenAlex
- W2113492975
- Cited by
- 291
- References
- 46
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 11 · 2023: 11 · 2022: 10 · 2021: 12 · 2020: 14 · 2019: 24 · 2018: 11 · 2017: 25 · 2016: 14 · 2015: 19 · 2014: 18 · 2013: 35 · 2012: 26
- FWCI
- 15.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- American Journal of Clinical Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- UEA Digital Repository (University of East Anglia) (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Dutch Diabetes Research Foundation (20060052)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Keywords
- saturated fatty acids, monounsaturated fatty acids, dietary fat composition, adipose tissue inflammation, metabolic syndrome, insulin sensitivity, gene expression profiles, oleic acid, LDL cholesterol, overweight, hyperinsulinemic-euglycemic clamp, cytokines
- MeSH terms
- Adipose Tissue, Adult, Aged, Complement C3, Fatty Acids, Female, Humans, Immunohistochemistry, Insulin Resistance, Lipids, Male, Middle Aged, Chemokine CCL5, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Metabolic Syndrome, PPAR gamma, Adiponectin
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