The interaction of short-chain fatty acids with adipose tissue: relevance for prevention of type 2 diabetes
Abstract
Short chain fatty acids (SCFA) are the main bacterial metabolites of colonic fermentation processes. The physiological relevance of the SCFA for the host outside the gastrointestinal tract is getting increased attention. In this review we will focus on the effect of SCFA on inflammation processes in the host in relation to insulin resistance. Obesity has been associated with a pro-inflammatory state of the adipose tissue that is associated with whole body insulin resistance leading to type 2 diabetes. Recently, two G protein-coupled receptors (GPCR) for SCFA, GPCR 41 and GPCR43, were described that are mainly expressed by immune cells but also by adipose tissue. Propionate can induce the satiety hormone leptin and reduce expression of inflammatory cytokines and chemokines indicating that SCFA have anti-inflammatory effects in human adipose tissue. In addition, in human nutritional experiments we observed that whole grain products could counteract a glucose-induced tumour necrosis factor α and interleukin-6 increase which was associated with increased plasma butyrate concentrations. This suggests that dietary fibre can produce a SCFA profile that could have anti-inflammatory effects in the body. The physiological relevance of these observations especially in relation to obesity-associated inflammation and insulin resistance is discussed.
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SCFAs can reduce inflammation.
“reduce inflammation [225]”
From The athletic gut microbiota (2020) · cites this paper as [225]
Cites
An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444 · see citing works
Metabolic Endotoxemia Initiates Obesity and Insulin Resistance
Cani, P. D., Amar, J., Iglesias, M. A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A. M., Fava, F., Tuohy, K. M., Chabo, C., et al. (2007) · Diabetes · doi:10.2337/db06-1491 · Cited by 6,638 · see citing works
Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43
Maslowski, K. M., Vieira, A. T., Ng, A., Kranich, J., Sierro, F., Yu, D., Schilter, H. C., Rolph, M. S., Mackay, F., Artis, D., et al. (2009) · Nature · doi:10.1038/nature08530 · Cited by 3,241 · see citing works
Turnbaugh, P. J., Bäckhed, F., Fulton, L., & Gordon, J. I. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.02.015 · Cited by 2,915 · see citing works
Energy contributions of volatile fatty acids from the gastrointestinal tract in various species
Bergman, E. N. (1990) · Physiological Reviews · doi:10.1152/physrev.1990.70.2.567 · Cited by 2,750 · see citing works
Mechanisms underlying the resistance to diet-induced obesity in germ-free mice
Bäckhed, F., Manchester, J. K., Semenkovich, C. F., & Gordon, J. I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605374104 · Cited by 2,615 · see citing works
Brown, A. J., Goldsworthy, S. M., Barnes, A. A., Eilert, M. M., Tcheang, L., Daniels, D., Muir, A. I., Wigglesworth, M. J., Kinghorn, I., Fraser, N. J., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211609200 · Cited by 2,409 · see citing works
Butyrate improves insulin sensitivity and increases energy expenditure in mice
Gao, Z., Yin, J., Zhang, J., Ward, R. E., Martin, R. J., Lefevre, M., Cefalu, W. T., & Ye, J. (2009) · Diabetes · doi:10.2337/db08-1637 · Cited by 2,204 · see citing works
Le Poul, E., Loison, C., Struyf, S., Springael, J.-Y., Lannoy, V., Decobecq, M.-E., Brezillon, S., Dupriez, V., Vassart, G., Van Damme, J., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301403200 · Cited by 1,651 · see citing works
Samuel, B. S., Shaito, A., Motoike, T., Rey, F. E., Backhed, F., Manchester, J. K., Hammer, R. E., Williams, S. C., Crowley, J., Yanagisawa, M., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808567105 · Cited by 1,564 · see citing works
Ahima, R. S., & Flier, J. S. (2000) · Annual Review of Physiology · doi:10.1146/annurev.physiol.62.1.413 · Cited by 1,428 · see citing works
Butyrate inhibits inflammatory responses through NFκB inhibition: implications for Crohn's disease
Segain, J.-P., de la Blétière, D. R., Bourreille, A., Leray, V., Gervois, N., Rosales, C., Ferrier, L., Bonnet, C., Blottière, H. M., & Galmiche, J.-P. (2000) · Gut · doi:10.1136/gut.47.3.397 · Cited by 1,325 · see citing works
Signals That Regulate Food Intake and Energy Homeostasis
Woods, S. C., Seeley, R. J., Porte, D., & Schwartz, M. W. (1998) · Science · doi:10.1126/science.280.5368.1378 · Cited by 1,169 · see citing works
The weight of leptin in immunity
Cava, A. L., & Matarese, G. (2004) · Nature Reviews Immunology · doi:10.1038/nri1350 · Cited by 927 · see citing works
Tedelind, S., Westberg, F., Kjerrulf, M., & Vidal, A. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i20.2826 · Cited by 856 · see citing works
Xiong, Y., Miyamoto, N., Shibata, K., Valasek, M. A., Motoike, T., Kedzierski, R. M., & Yanagisawa, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2637002100 · Cited by 731 · see citing works
Acetate and Propionate Short Chain Fatty Acids Stimulate Adipogenesis via GPCR43
Hong, Y.-H., Nishimura, Y., Hishikawa, D., Tsuzuki, H., Miyahara, H., Gotoh, C., Choi, K.-C., Feng, D. D., Chen, C., Lee, H.-G., et al. (2005) · Endocrinology · doi:10.1210/en.2005-0545 · Cited by 613 · see citing works
Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults
Pereira, M. A., Jacobs, D. R., Pins, J. J., Raatz, S. K., Gross, M. D., Slavin, J. L., & Seaquist, E. R. (2002) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/75.5.848 · Cited by 544 · see citing works
The metabolic syndrome and adipocytokines
Matsuzawa, Y. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.04.028 · Cited by 541 · see citing works
Ge, H., Li, X., Weiszmann, J., Wang, P., Baribault, H., Chen, J., Tian, H., & Li, Y. (2008) · Endocrinology · doi:10.1210/en.2008-0059 · Cited by 477 · see citing works
An immune origin of type 2 diabetes?
Kolb, H., & Mandrup-Poulsen, T. (2005) · Diabetologia · doi:10.1007/s00125-005-1764-9 · Cited by 394 · see citing works
Oligofructose Promotes Satiety in Rats Fed a High‐Fat Diet: Involvement of Glucagon‐Like Peptide‐1
Cani, P. D., Neyrinck, A. M., Maton, N., & Delzenne, N. M. (2005) · Obesity Research · doi:10.1038/oby.2005.117 · Cited by 382 · see citing works
Oligofructose promotes satiety in healthy human: a pilot study
Cani, P. D., Joly, E., Horsmans, Y., & Delzenne, N. M. (2005) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602350 · Cited by 381 · see citing works
Short-chain fatty acids act as antiinflammatory mediatorsby regulating prostaglandin E2 and cytokines
Cox, M. A., Jackson, J., Stanton, M., Rojas-Triana, A., Bober, L., Laverty, M., Yang, X., Zhu, F., Liu, J., Wang, S., et al. (2009) · World Journal of Gastroenterology · doi:10.3748/wjg.15.5549 · Cited by 377 · see citing works
Salsalate Improves Glycemia and Inflammatory Parameters in Obese Young Adults
Fleischman, A., Shoelson, S. E., Bernier, R., & Goldfine, A. B. (2008) · Diabetes Care · doi:10.2337/dc07-1338 · Cited by 352 · see citing works
Effects of Resistant Starch, A Non‐digestible Fermentable Fiber, on Reducing Body Fat
Keenan, M. J., Zhou, J. F., McCutcheon, K. L., Raggio, A. M., Bateman, H. G., Todd, E., Jones, C. K., Tulley, R. T., Melton, S. A., Martin, R. J., et al. (2006) · Obesity · doi:10.1038/oby.2006.176 · Cited by 300 · see citing works
Fat as an Endocrine Organ: Relationship to the Metabolic Syndrome
Hutley, L. J., & Prins, J. B. (2005) · The American Journal of the Medical Sciences · doi:10.1097/00000441-200512000-00005 · Cited by 258 · see citing works
Characterization of the Human Visceral Adipose Tissue Secretome
Álvarez‐Llamas, G., Szalowska, E., de Vries, M. P., Weening, D., Landman, K., Hoek, A., Wolffenbuttel, B. H. R., Roelofsen, H., & Vonk, R. J. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600265-mcp200 · Cited by 231 · see citing works
Self-citationRegulation of adipokine production in human adipose tissue by propionic acid
Al-Lahham, S., Roelofsen, H., Priebe, M. G., Weening, D., Dijkstra, M., Hoek, A., Rezaee, F., Venema, K., & Vonk, R. J. (2010) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2010.02278.x · Cited by 222 · see citing works
Self-citationGarcia, A. L., Otto, B., Reich, S.-C., Weickert, M. O., Steiniger, J., Machowetz, A., Rudovich, N. N., Möhlig, M., Katz, N., Speth, M., et al. (2007) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602525 · Cited by 203 · see citing works
Adipose tissue as an active endocrine organ: recent advances
Gimeno, R. E., & Klaman, L. D. (2005) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2005.01.006 · Cited by 180 · see citing works
Whole grain foods for the prevention of type 2 diabetes mellitus
Priebe, M. G., van Binsbergen, J., de Vos, R., & Vonk, R. J. (2008) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd006061.pub2 · Cited by 142 · see citing works
Self-citationZapolska‐Downar, D., Siennicka, A., Kaczmarczyk, M., Kołodziej, B., & Naruszewicz, M. (2004) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2003.11.008 · Cited by 140 · see citing works
Koška, J., Ortega, E., Bunt, J. C., Gasser, A., Impson, J., Hanson, R. L., Forbes, J. M., de Courten, B. V., & Krakoff, J. A. (2008) · Diabetologia · doi:10.1007/s00125-008-1239-x · Cited by 119 · see citing works
Nilsson, A. C., Granfeldt, Y. E., Östman, E. M., Preston, T., & Björck, I. (2006) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602423 · Cited by 101 · see citing works
Nilsson, A. C., Östman, E. M., Preston, T., & Björck, I. (2007) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602784 · Cited by 93 · see citing works
Priebe, M. G., Wang, H., Weening, D., Schepers, M., Preston, T., & Vonk, R. J. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.28521 · Cited by 91 · see citing works
Self-citationDietary Resistant Starch Increases Hypothalamic POMC Expression in Rats
Shen, L., Keenan, M. J., Martin, R. J., Tulley, R. T., Raggio, A. M., McCutcheon, K. L., & Zhou, J. (2008) · Obesity · doi:10.1038/oby.2008.483 · Cited by 87 · see citing works
Zapolska‐Downar, D., & Naruszewicz, M. (2009) · PubMed · Cited by 74 · see citing works
Coordinate regulation of ovine adipose tissue gene expression by propionate
Lee, S. H., & HOSSNER, K. L. (2002) · Journal of Animal Science · doi:10.2527/2002.80112840x · Cited by 65 · see citing works
Soliman, M. M., Kimura, K., Ahmed, M. M., Yamaji, D., Matsushita, Y., Okamatsu‐Ogura, Y., Makondo, K. J., & Saito, M. (2006) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2006.08.005 · Cited by 63 · see citing works
Zhou, J., Martin, R. J., Tulley, R. T., Raggio, A. M., Shen, L., Lissy, E., McCutcheon, K. L., & Keenan, M. J. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf901548e · Cited by 61 · see citing works
Roelofsen, H., Dijkstra, M., Weening, D., de Vries, M. P., Hoek, A., & Vonk, R. J. (2008) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m800254-mcp200 · Cited by 49 · see citing works
Self-citationAssociation of 1,5-Anhydroglucitol and 2-h Postprandial Blood Glucose in Type 2 Diabetic Patients
Schindhelm, R. K., Diamant, M., Bilo, H. J. G., et al. (2008) · Diabetes Care · doi:10.2337/dc08-1399 · Cited by 8 · see citing works
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Tan, J., McKenzie, C., Potamitis, M., Thorburn, A. N., Mackay, C. R., & Macia, L. (2014) · Advances in immunology · doi:10.1016/b978-0-12-800100-4.00003-9 · Cited by 2,425 · see citing works
Short chain fatty acids in human gut and metabolic health
Blaak, E. E., Canfora, E. E., Theis, S., Frost, G., Groen, A. K., Mithieux, G., Nauta, A., Scott, K., Stahl, B., van Harsselaar, J., et al. (2020) · Beneficial Microbes · doi:10.3920/bm2020.0057 · Cited by 1,103 · see citing works
Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice
Le Roy, T., Llopis, M., Lepage, P., Bruneau, A., Rabot, S., Bevilacqua, C., Martin, P., Philippe, C., Walker, F., Bado, A., et al. (2013) · Gut · doi:10.1136/gutjnl-2012-303816 · Cited by 1,001 · see citing works
Exercise alters gut microbiota composition and function in lean and obese humans
ALLEN, J. M., MAILING, L. J., NIEMIRO, G. M., MOORE, R., COOK, M. D., WHITE, B. A., HOLSCHER, H. D., & WOODS, J. A. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001495 · Cited by 820 · see citing works
Mohr, A. E., Jäger, R., Carpenter, K. C., Kerksick, C. M., Purpura, M., Townsend, J. R., West, N. P., Black, K., Gleeson, M., Pyne, D. B., et al. (2020) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-020-00353-w · Cited by 378 · see citing works
“SCFAs can improve skeletal muscle insulin sensitivity [224], reduce inflammation [225], and regulate satiety [226], all of which may contribute to the improvements in body composition observed in this study.”
BackgroundHe, B., Hoang, T. K., Wang, T., Ferris, M., Taylor, C. M., Tian, X., Luo, M., Tran, D. Q., Zhou, J., Tatevian, N., et al. (2017) · Journal of Experimental Medicine · doi:10.1084/jem.20160961 · Cited by 196 · see citing works
- Authors
- Roelofsen, H., Priebe, M., & Vonk, R.
- Affiliations
- University Medical Center Groningen (NL)
- ORCID
- Priebe, M.
- Venue
- Beneficial Microbes
- Publisher
- Walter de Gruyter GmbH
- Published
- 2010-11-01
- Volume
- 1
- Issue
- 4
- Pages
- 433-438
- ISSN
- 1876-2883 (ISSN-L)
- 1876-2891
- OpenAlex
- W1986350670
- Cited by
- 80
- References
- 44
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 3 · 2021: 7 · 2020: 13 · 2019: 4 · 2018: 6 · 2017: 5 · 2016: 7 · 2015: 4 · 2014: 6 · 2013: 5 · 2012: 4
- FWCI
- 0.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Beneficial Microbes (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Keywords
- short-chain fatty acids, adipose tissue, type 2 diabetes prevention, insulin resistance, obesity, inflammation, GPR41, GPR43, butyrate, leptin, dietary fiber, whole grains, TNF-α, interleukin-6, colonic fermentation, gut microbiota metabolites
- MeSH terms
- Adipose Tissue, Animals, Bacteria, Diabetes Mellitus, Type 2, Fatty Acids, Volatile, Humans, Insulin Resistance, Gastrointestinal Tract, Metagenome
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