Skip to main content
×
Home

Obesity, inflammation and the immune system

  • Fátima Pérez de Heredia (a1), Sonia Gómez-Martínez (a1) and Ascensión Marcos (a1)
Abstract

Obesity shares with most chronic diseases the presence of an inflammatory component, which accounts for the development of metabolic disease and other associated health alterations. This inflammatory state is reflected in increased circulating levels of pro-inflammatory proteins, and it occurs not only in adults but also in adolescents and children. The chronic inflammatory response has its origin in the links existing between the adipose tissue and the immune system. Obesity, like other states of malnutrition, is known to impair the immune function, altering leucocyte counts as well as cell-mediated immune responses. In addition, evidence has arisen that an altered immune function contributes to the pathogenesis of obesity. This review attempts to briefly comment on the various plausible explanations that have been proposed for the phenomenon: (1) the obesity-associated increase in the production of leptin (pro-inflammatory) and the reduction in adiponectin (anti-inflammatory) seem to affect the activation of immune cells; (2) NEFA can induce inflammation through various mechanisms (such as modulation of adipokine production or activation of Toll-like receptors); (3) nutrient excess and adipocyte expansion trigger endoplasmic reticulum stress; and (4) hypoxia occurring in hypertrophied adipose tissue stimulates the expression of inflammatory genes and activates immune cells. Interestingly, data suggest a greater impact of visceral adipose tissue and central obesity, rather than total body fat, on the inflammatory process. In summary, there is a positive feedback loop between local inflammation in adipose tissue and altered immune response in obesity, both contributing to the development of related metabolic complications.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Obesity, inflammation and the immune system
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Obesity, inflammation and the immune system
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Obesity, inflammation and the immune system
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Dr Fátima Pérez de Heredia, fax +34 915493627, email fatima.perezdeheredia@ictan.csic.es
References
Hide All
1.Gorman C, Park A & Dell K (2004) Health: the fires within. Time (23 February, USA edition) 163(8), 3845.
2.Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444, 860867.
3.Bastard JP, Maachi M, Lagathu C et al. (2006) Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17, 4–12.
4.Festa A, D'Agostino R Jr, Williams K et al. . (2001) The relation of body fat mass and distribution to markers of chronic inflammation. Int J Obes Relat Metab Disord 25, 14071415.
5.Park HS, Park JY & Yu R (2005) Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-alpha and IL-6. Diabetes Res Clin Pract 69, 2935.
6.Bulló M, García-Lorda P, Megias I et al. (2003) Systemic inflammation, adipose tissue tumor necrosis factor, and leptin expression. Obes Res 11, 525531.
7.Hermsdorff HH, Zulet MA, Puchau B et al. (2011) Central adiposity rather than total adiposity measurements are specifically involved in the inflammatory status from healthy young adults. Inflammation 34, 161170.
8.Lapice E, Maione S, Patti L et al. (2009) Abdominal adiposity is associated with elevated C-reactive protein independent of BMI in healthy nonobese people. Diabetes Care 32, 17341736.
9.Wajchenberg BL (2000) Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 21, 697738.
10.Wärnberg J, Nova E, Romeo J et al. (2007) Lifestyle-related determinants of inflammation in adolescence. Br J Nutr 98, Suppl. 1, S116S120.
11.Quijada Z, Paoli M, Zerpa Y et al. (2008) The triglyceride/HDL-cholesterol ratio as a marker of cardiovascular risk in obese children; association with traditional and emergent risk factors. Pediatr Diabetes 9, 464471.
12.Weiss R, Dziura J, Burgert TS et al. (2004) Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 350, 23622374.
13.Halle M, Korsten-Reck U, Wolfarth B et al. (2004) Low-grade systemic inflammation in overweight children: impact of physical fitness. Exerc Immunol Rev 10, 6674.
14.Reinehr T, Stoffel-Wagner B, Roth CL et al. (2005) High-sensitive C-reactive protein, tumor necrosis factor alpha, and cardiovascular risk factors before and after weight loss in obese children. Metabolism 54, 11551161.
15.Gupta A, Ten S & Anhalt H (2005) Serum levels of soluble tumor necrosis factor-alpha receptor 2 are linked to insulin resistance and glucose intolerance in children. J Pediatr Endocrinol Metab 18, 7582.
16.Aeberli I, Molinari L, Spinas G et al. (2006) Dietary intakes of fat and antioxidant vitamins are predictors of subclinical inflammation in overweight Swiss children. Am J Clin Nutr 84, 748755.
17.Giordano P, Del Vecchio GC, Cecinati V et al. (2011) Metabolic, inflammatory, endothelial and haemostatic markers in a group of Italian obese children and adolescents. Eur J Pediatr 170, 845850.
18.Gøbel RJ, Jensen SM, Frøkiaer H et al. (2012) Obesity, inflammation and metabolic syndrome in Danish adolescents. Acta Paediatr 101(2), 192200.
19.Wärnberg J, Nova E, Moreno LA et al. (2006) Inflammatory proteins are related to total and abdominal adiposity in a healthy adolescent population: the AVENA Study. Am J Clin Nutr 84, 505512.
20.Martínez-Gómez D, Eisenmann JC, Wärnberg JA et al. (2010) Associations of physical activity, fitness and fatness with low-grade inflammation in adolescents. The AFINOS study. Int J Obes (London) 34, 15011507.
21.Ruiz JR, Ortega FB, Warnberg J et al. (2007) Associations of low-grade inflammation with physical activity, fitness and fatness in prepubertal children; the European Youth Heart Study. Int J Obes (Lond) 31, 15451551.
22.Romeo J, Martínez-Gómez D, Díaz LE et al. (2011) Changes in cardiometabolic risk factors, appetite-controlling hormones and cytokines after a treatment programme in overweight adolescents: preliminary findings from the EVASYON study. Pediatric Diabetes 12, 372380.
23.Martí A, Marcos A & Martínez JA (2001) Obesity and immune function relationships. Obes Rev 2, 131140.
24.Sheridan PA, Paich HA, Handy J et al. (2011) Obesity is associated with impaired immune response to influenza vaccination in humans. Int J Obes (Lond), doi: 10.1038/ijo.2011.208. (Epublication ahead of print version).
25.Caspar-Bauguil S, Cousin B, Galinier A et al. (2005) Adipose tissues as an ancestral immune organ: site-specific change in obesity. FEBS Lett 579, 34873492.
26.Saely CH, Geiger K & Drexel H (2010) Brown versus white adipose tissue: a mini-review. Gerontology 58(1), 1523.
27.Poglio S, de Toni-Costes F, Arnaud E et al. (2010) Adipose tissue as a dedicated reservoir of functional mast cell progenitors. Stem Cells 28, 20652072.
28.Weisberg SP, McCann D, Desai M et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112, 17961808.
29.Lumeng CN, Bodzin JL & Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117, 175184.
30.Odegaard JI, Ricardo-González RR, Goforth MH et al. (2007) Macrophage-specific PPAR-gamma controls alternative activation and improves insulin resistance. Nature 447, 11161120.
31.Trayhurn P & Wood IS (2004) Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr 92, 347355.
32.Tilg H & Moschen AR (2006) Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nature 6, 772783.
33.Koerner A, Kratzsch J & Kiess W (2005) Adipocytokines: leptin – the classical, resistin – the controversial, adiponectin – the promising, and more to come. Best Pract Res Clin Endocrinol Metab 19, 525546.
34.Virtue S & Vidal-Puig A (2010) Adipose tissue expandability, lipotoxicity and the metabolic syndrome – an allostatic perspective. Biochim Biophys Acta 1801, 338349.
35.Pietiläinen KH, Róg T, Seppänen-Laakso T et al. (2011) Association of lipidome remodeling in the adipocyte membrane with acquired obesity in humans. PLoS Biol 9, e1000623.
36.Stryjecki C & Mutch DM (2011) Fatty acid-gene interactions, adipokines and obesity. Eur J Clin Nutr 65, 285297.
37.Suganami T, Tanimoto-Koyama K, Nishida J et al. (2007) Role of the toll-like receptor 4/NF-kappa B pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler Thromb Vasc Biol 27, 8491.
38.Fernández-Real JM, Vendrell J & Ricart W (2005) Circulating adiponectin and plasma fatty acid profile. Clin Chem 51, 603609.
39.Pérez de Heredia F, Sánchez J, Priego T et al. (2009) Adiponectin is associated with serum and adipose tissue fatty acid composition in rats. J Endocrinol Invest 32, 659665.
40.Coll T, Barroso E, Álvarez-Guardia D et al. (2010) The role of peroxisome proliferator-activated receptor beta/delta on the inflammatory basis of metabolic disease. PPAR Res, pii, 368467.
41.Fessler MB, Rudel LL & Brown JM (2009) Toll-like receptor signaling links dietary fatty acids to the metabolic syndrome. Curr Opin Lipidol 20, 379385.
42.Grunfeld C & Feingold KR (1991) The metabolic effects of tumor necrosis factor and other cytokines. Biotherapy 3, 143158.
43.Mei M, Zhao L, Li Q et al. (2011) Inflammatory stress exacerbates ectopic lipid deposition in C57BL/6J mice. Lipids Health Dis 10, 110 (Epublication ahead of print version).
44.Gregor MF & Hotamisligil GS (2007) Thematic review series: Adipocyte biology. adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 48, 19051914.
45.Trayhurn P, Pérez de Heredia F, Wang B et al. (2010) Hypoxia – role in adipocyte function and dysfunction. In Novel Insight into Adipose Cell Functions, pp. 4560 [Clément K, Spiegelman BM and Christen Y, editors]. Berlin, Heidelberg: Springer-Verlag.
46.Pérez de Heredia F, Wood IS & Trayhurn P (2010) Hypoxia stimulates lactate release and modulates monocarboxylate transporter (MCT1, MCT2, MCT4) expression in human adipocytes. Pflüg Arch – Eur J Physiol 459, 509518.
47.Samuvel DJ, Sundararaj KP, Nareika A et al. (2009) Lactate boosts TLR4 signaling and NF-ΚB pathway-mediated gene transcription in macrophages via monocarboxylate transporters and MD-2 up-regulation. J Immunol 182, 24762484.
48.Pérez de Heredia F, Wood IS & Trayhurn P (2010) Lactate enhances the inflammatory response in human preadipocytes in vitro. Obes Rev 11, Suppl. 1, 122 (Abstract).
49.Halberg N, Khan T, Trujillo ME et al. (2009) Hypoxia-inducible factor 1α induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol 29, 44674483.
50.Cancello R, Tordjman J, Poitou C et al. (2006) Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes 55, 15541561.
51.Hernández-Morante JJ, Milagro F, Gabaldón JA et al. (2006) Effect of DHEA-sulfate on adiponectin gene expression in adipose tissue from different fat depots in morbidly obese humans. Eur J Endocrinol 155, 593600.
52.Villaret A, Galitzky J, Decaunes P et al. (2010) Adipose tissue endothelial cells from obese human subjects: differences among depots in angiogenic, metabolic, and inflammatory gene expression and cellular senescence. Diabetes 59, 27552763.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Proceedings of the Nutrition Society
  • ISSN: 0029-6651
  • EISSN: 1475-2719
  • URL: /core/journals/proceedings-of-the-nutrition-society
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 341
Total number of PDF views: 932 *
Loading metrics...

Abstract views

Total abstract views: 2121 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 24th November 2017. This data will be updated every 24 hours.