Journal of Physiology and Biochemistry

, Volume 68, Issue 4, pp 701–711 | Cite as

Oxidative stress and inflammation interactions in human obesity

  • Isabel Bondia-Pons
  • Lisa Ryan
  • J. Alfredo Martinez
Mini Review

Abstract

Obesity is often characterized by increased oxidative stress and exacerbated inflammatory outcomes accompanying infiltration of immune cells in adipocytes. The oxidative stress machinery and inflammatory signaling are not only interrelated, but their impairment can lead to an inhibition of insulin responses as well as a higher risk of cardiovascular diseases and associated features. Mitochondria, in addition to energy transformation, play a role in apoptosis, cellular proliferation, as well as in the cellular redox state control. Under certain circumstances, protons are able to re-enter the mitochondrial matrix via different uncoupling proteins, disturbing free radical production by mitochondria. Disorders of the mitochondrial electron transport chain, over-generation of reactive oxygen species, and lipoperoxides or alterations in antioxidant defenses have been reported in situations of obesity and type-2 diabetes. On the other hand, obesity has been linked to a low grade pro-inflammatory state, in which impairments in the oxidative stress and antioxidant mechanism could be involved. The current scientific evidence highlights the need of investigating the interplay between oxidative stress and inflammation with obesity/diabetes onset as well as the interactions of such factors either as a cause or consequence of obesity. The signaling mediated by the activation of inflammatory markers or nuclear factor kappa β and other transcription factors as central regulators of inflammation are key issues to understanding oxidative stress responses in obesity. This review aims at summarizing the main mechanisms and interplay factors between oxidative stress and inflammation in human obesity according to the last 10 years of research in the field.

Keywords

Obesity Inflammation Oxidative stress Cytokines Hypoxia 

References

  1. 1.
    Atkinson RL (2007) Viruses as an etiology of obesity. Mayo Clin Proc 82:1192–1198PubMedGoogle Scholar
  2. 2.
    Atkinson RL, Dhurandhar NV, Allison DB, Bowen RL, Israel BA, Albu JB, Augustus AS (2005) Human adenovirus-36 is associated with increased body weight and paradoxical reduction of serum lipids. Int J Obes 29(3):281–286Google Scholar
  3. 3.
    Baker RG, Hayden MS, Ghosh S (2011) NF-κB, inflammation, and metabolic disease. Cell Metab 13:11–22PubMedGoogle Scholar
  4. 4.
    Barnes KM, Miner JL (2009) Role of resistin in insulin sensitivity in rodents and humans. Curr Protein Pept Sci 10:96–107PubMedGoogle Scholar
  5. 5.
    Berthier MT, Paradis AM, Tchernof A et al (2003) The interleukin 6–174 G/C polymorphism is associated with indices of obesity in men. J Hum Genet 48:14–19PubMedGoogle Scholar
  6. 6.
    Bogani P, Galli C, Villa M, Visioli F (2007) Postprandial anti-inflammatory and antioxidant effects of extra virgin olive oil. Atherosclerosis 190:181–186PubMedGoogle Scholar
  7. 7.
    Calder PC (2006) n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83:1505S–1519SPubMedGoogle Scholar
  8. 8.
    Calder PC, Albers R, Antoine JM, Blum S, Bourdet-Sicard R, Ferns GA, Folkerts G, Friedmann PS, Frost GS, Guarner F, Løvik M, Macfarlane S, Meyer PD, M'Rabet L, Serafini M, van Eden W, van Loo J, Vas Dias W, Vidry S, Winklhofer-Roob BM, Zhao J (2009) Inflammatory disease processes and interactions with nutrition. Br J Nutr 101(Suppl 1):S1–45PubMedGoogle Scholar
  9. 9.
    Cancello R, Henegar C, Viguerie N, Taleb S, Poitou C, Rouault C et al (2005) Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 54:2277–2286PubMedGoogle Scholar
  10. 10.
    Carp R, Meeker H, Sersen E, Kozlowski P (1998) Analysis of the incubation periods, induction of obesity and histopathological changes in senescence-prone and senescence-resistant mice infected with various scrapie strains. J Gen Virol 79:2863–2869PubMedGoogle Scholar
  11. 11.
    Carter JK, Ow CL, Smith RE (1983) Rous-associated virus type 7 induces a syndrome in chickens characterized by stunting and obesity. Infect Immun 39:410–422PubMedGoogle Scholar
  12. 12.
    Ceriello A, Motz E (2004) Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 24:816–823PubMedGoogle Scholar
  13. 13.
    Correia ML, Haynes WG (2006) A role for plasminogen activator inhibitor-1 in obesity: from pie to PAI? Arterioscler Thromb Vasc Biol 26:2183–2185PubMedGoogle Scholar
  14. 14.
    Curti ML, Jacob P, Borges MC, Rogero MM, Ferreira SR (2011) Studies of gene variants related to inflammation, oxidative stress, dyslipidemia, and obesity: implications for a nutrigenetic approach. J Obes (in press)Google Scholar
  15. 15.
    Dalgaard LT (2011) Genetic variance in uncoupling protein 2 in relation to obesity. Type 2 diabetes, and related metabolic traits: focus on the functional 866 G > A promoter variant (rs659366). J Obes (in press)Google Scholar
  16. 16.
    Deeb SS, Fajas L, Nemoto M, Pihlajamäki J, Mykkänen L, Kuusisto J, Laakso M, Fujimoto W, Auwerx J (1998) A Pro12Ala substitution in PPARγ2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivity. Nature Genet 20:284–287PubMedGoogle Scholar
  17. 17.
    De Nardo D, Latz E (2011) NLRP3 inflammasomes link inflammation and metabolic disease. Trends Immunol 32:373–379PubMedGoogle Scholar
  18. 18.
    Del Rio D, Agnoli C, Pellegrini N, Krogh V, Brighenti F, Mazzeo T, Masala G, Bendinelli B, Berrino F, Sieri S, Tumino R, Rollo PC, Gallo V, Sacerdote C, Mattiello A, Chiodini P, Panico S (2011) Total antioxidant capacity of the diet is associated with lower risk of ischemic stroke in a large Italian cohort. J Nutr 141:118–123PubMedGoogle Scholar
  19. 19.
    Dhurandhar NV, Israel BA, Kolesar JM, Mayhew GF, Cook ME, Atkinson RL (2000) Increased adiposity in animals due to a human virus. Int J Obes Relat Metab Disord 24:989–996PubMedGoogle Scholar
  20. 20.
    Dina C, Meyre D, Gallina S, Durand E et al (2007) Variation in FTO contributes to childhood obesity and severe adult obesity. Nat Genet 39:724–726PubMedGoogle Scholar
  21. 21.
    Elmarakby AA, Sullivan JC (2010) Relationship between oxidative stress and inflammatory cytokines in diabetic nephropathy. Cardiovasc Ther 00:1–11Google Scholar
  22. 22.
    Estruch R (2010) Anti-inflammatory effects of the Mediterranean diet: the experience of the PREDIMED study. Proc Nutr Soc 69:333–340PubMedGoogle Scholar
  23. 23.
    Estruch R, Martinez-Gonzalez MA, Corella D, Salas-Salvadó J, Ruiz-Gutiérrez V, Covas MI, Fiol M, Gómez-Gracia E, López-Sabater MC, Vinyoles E, Arós F, Conde M, Lahoz C, Lapetra J, Sáez G, Ros E, PREDIMED Study Investigators (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145:1–11PubMedGoogle Scholar
  24. 24.
    Feinberg AP, Irizarry RA, Fradin D, Aryee MJ, Murakami P, Aspelund T, Eiriksdottir G, Harris TB, Launer L, Gudnason V, Fallin MD (2010) Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci Transl Med 2:49–67Google Scholar
  25. 25.
    Fernandez-Real JM, Ricart W (2003) Insulin resistance and chronic cardiovascular inflammatory syndrome. Endocr Rev 24:278–301PubMedGoogle Scholar
  26. 26.
    Fortuño A, Rodríguez A, Gómez-Ambrosi J, Frühbeck G, Díez J (2003) Adipose tissue as an endocrine organ: role of leptin and adiponectin in the pathogenesis of cardiovascular diseases. J Physiol Biochem 59:51–60PubMedGoogle Scholar
  27. 27.
    Frayling TM, Timpson NJ, Weedon MN et al (2007) A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 316:889–894PubMedGoogle Scholar
  28. 28.
    Frederiksen L, Brødbæk K, Fenger M et al (2002) Comment: studies of the Pro12Ala polymorphism of the PPAR-γ gene in the Danish MONICA cohort: homozygosity of the Ala allele confers a decreased risk of the insulin resistance syndrome. J Clin Endocrinol Metab 87:3989–3992PubMedGoogle Scholar
  29. 29.
    Furukawa S, Fujita K, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114:1752–1761PubMedGoogle Scholar
  30. 30.
    Ghoussaini M, Meyre D, Lobbens S, Charpentier G, Clément K, Charles MA, Tauber M, Weill J, Froguel P (2005) Implication of the Pro12Ala polymorphism of the PPAR-gamma 2 gene intype 2 diabetes and obesity in the French population. BMC Medical Genetics 6:11PubMedGoogle Scholar
  31. 31.
    Goossens GH (2008) The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav 94:206–218PubMedGoogle Scholar
  32. 32.
    Goyenechea E, Parra MD, Martinez JA (2005) Role ofIL-6 and its -174 G > C polymorphism in weight management and in the metabolic comorbidities associated with obesity. Implicación de la IL-6 y su polimorfismo -174 G/C en el control del peso corporal y en las complicaciones metabólicas asociadas a la obesidad. Anales del Sistema Sanitario de Navarra 28:357–366PubMedGoogle Scholar
  33. 33.
    Gregor MF, Hotamisligil GS (2007) Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 48:1905–1914PubMedGoogle Scholar
  34. 34.
    Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Förster I, Farlik M, Decker T, Du Pasquier RA, Romero P, Tschopp J (2011) Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34:213–223PubMedGoogle Scholar
  35. 35.
    Gutcher I, Becher B (2007) C-derived cytokines and T cell polarization in autoimmune inflammation. J Clin Invest 117:1119–1127PubMedGoogle Scholar
  36. 36.
    Harford KA, Reynolds CM, McGillicuddy FC, Roche HM (2011) Fats, inflammation and insulin resistance: insights to the role of macrophage and T-cell accumulation in adipose tissue. Proc Nutr Soc 12:1–10Google Scholar
  37. 37.
    Henze K, Martin W (2003) Evolutionary biology: essence of mitochondria. Nature 426:127–128*PubMedGoogle Scholar
  38. 38.
    Hermsdorff HH, Zulet MÁ, Abete I, Martínez JA (2009) Discriminated benefits of a Mediterranean dietary pattern within a hypocaloric diet program on plasma RBP4 concentrations and other inflammatory markers in obese subjects. Endocrine 36:445–451PubMedGoogle Scholar
  39. 39.
    Hopps E, Noto D, Caimi G, Averna MR (2010) A novel component of the metabolic syndrome: the oxidative stress. Nutr Metab Cardiovasc Dis 20:72–77PubMedGoogle Scholar
  40. 40.
    Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860–867PubMedGoogle Scholar
  41. 41.
    Hotamisligil GS, Erbay E (2008) Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol 8:923–934PubMedGoogle Scholar
  42. 42.
    Hotamisligil GS, Spiegelman BM (1994) Tumor necrosis factor alpha: a key component of the obesity diabetes link. Diabetes 43:1271–1278PubMedGoogle Scholar
  43. 43.
    Houstis N, Rosen ED, Lander ES (2006) Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440:944–948PubMedGoogle Scholar
  44. 44.
    Jia JJ, Zhang X, Ge CR, Jois M (2009) The polymorphisms of UCP2 and UCP3 genes associated with fat metabolism, obesity and diabetes. Obes Rev 10:519–526PubMedGoogle Scholar
  45. 45.
    Jones AB (2001) Peroxisome proliferator-activated receptor (PPAR) modulators: diabetes and beyond. Med Res Rev 21:540–552PubMedGoogle Scholar
  46. 46.
    Kanneganti TD (2010) Central roles of NLRs and inflammasomes in viral infection. Nat Rev Immunol 10:688–698PubMedGoogle Scholar
  47. 47.
    Karalis KP, Giannogonas P, Kodela E, Koutmani Y, Zoumakis M, Teli T (2009) Mechanisms of obesity and related pathology: linking immune responses to metabolic stress. FEBS J 276:5747–5754PubMedGoogle Scholar
  48. 48.
    Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M, Wabitsch M, Fischer-Posovszky P, Barth TF, Dragun D, Skurk T, Hauner H, Blüher M, Unger T, Wolf AM, Knippschild U, Hombach V, Marx N (2008) T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler Thromb Vasc Biol 28:1304–1310PubMedGoogle Scholar
  49. 49.
    Klipstein-Grobusch K, Möhlig M, Spranger J, Hoffmann K, Rodrigues FU, Sharma AM, Klaus S, Pfeiffer AF, Boeing H (2006) Interleukin-6 g.-174G>C promoter polymorphism is associated with obesity in the EPIC-Potsdam study. Obesity 14:14–18PubMedGoogle Scholar
  50. 50.
    Kolonin MG, Saha PK, Chan L, Pasqualini R, Arap W (2004) Reversal of obesity by targeted ablation of adipose tissue. Nat Med 10:625–632PubMedGoogle Scholar
  51. 51.
    Krzystek-Korpacka M, Patryn E, Boehm D, Berdowska I, Zielinski B, Noczynska A (2008) Advanced oxidation protein products (AOPPs) in juvenile overweight and obesity prior to and following weight reduction. Clin Biochem 41:943–949PubMedGoogle Scholar
  52. 52.
    Kusminski CM, McTernan PG, Kumar S (2005) Role of resistin in obesity, insulin resistance and type II diabetes. Clin Sci (Lond) 109:243–256Google Scholar
  53. 53.
    Lamkanfi M, Kanneganti TD (2010) Nlrp3: an immune sensor of cellular stress and infection. Int J Biochem Cell Biol 42:792–795PubMedGoogle Scholar
  54. 54.
    Latvala S, Miettinen M, Kekkonen RA, Korpela R, Julkunen I (2011) Lactobacillus rhamnosus GG and Streptococcus thermophilus induce suppressor of cytokine signalling 3 (SOCS3) gene expression directly and indirectly via interleukin-10 in human primary macrophages. Clin Exp Immunol 165:94–103PubMedGoogle Scholar
  55. 55.
    Loos RJ, Lindgren CM, Li S, Wheeler E et al (2008) Common variants near MC4R are associated with fat mass, weight and risk of obesity. Nat Genet 40:768–775PubMedGoogle Scholar
  56. 56.
    Lowell BB, Shulman GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307:384–387PubMedGoogle Scholar
  57. 57.
    Lubis AR, Widia F, Soegondo S, Setiawati A (2008) The role of SOCS-3 protein in leptin resistance and obesity. Acta Med Indones 40:89–95PubMedGoogle Scholar
  58. 58.
    Lukens JR, Dixit VD, Kanneganti TD (2011) Inflammasome activation in obesity-related inflammatory diseases and autoimmunity. Discov Med 12:65–74PubMedGoogle Scholar
  59. 59.
    Lumeng CN, DelProposto JB, Westcott DJ, Saltiel AR (2008) Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 57:3239–3246PubMedGoogle Scholar
  60. 60.
    Lumeng CN, Saltiel AR (2011) Inflammatory links between obesity and metabolic disease. J Clin Invest 121:2111–2117PubMedGoogle Scholar
  61. 61.
    Lyons MJ, Faust IM, Hemmes RB, Buskirk DR, Hirsch J, Zabriskie JB (1982) A virally induced obesity syndrome in mice. Science 216:82–85PubMedGoogle Scholar
  62. 62.
    Mantovani A, Bonecchi R, Locati M (2006) Tuning inflammation and immunity by chemokine sequestration: decoys and more. Nat Rev Immunol 6:907–918PubMedGoogle Scholar
  63. 63.
    Marti A, Corbalán MS, Martínez-González MA, Forga L, Martínez JA (2002) CHO intake alters obesity risk associated with Pro12Ala polymorphism of PPAR gamma gene. J Physiol Biochem 58:219–220PubMedGoogle Scholar
  64. 64.
    Marti A, Goyenechea E, Martínez JA (2010) Nutrigenetics: a tool to provide personalized nutritional therapy to the obese. J Nutrigenet Nutrigenomics 3:157–169PubMedGoogle Scholar
  65. 65.
    Martínez JA (2006) Mitochondrial oxidative stress and inflammation: an slalom to obesity and insulin resistance. Physiol Biochem 62:303–306Google Scholar
  66. 66.
    Martinez-Hervas S, Mansego ML, de Marco G, Martinez F, Alonso MP, Morcillo S, Rojo-Martinez G, Real JT, Ascaso JF, Redon J, Martin Escudero JC, Soriguer F, Chaves FJ (2011) Polymorphisms of the UCP2 gene are associated with body fat distribution and risk of abdominal obesity in Spanish population. Eur J Clin Invest (in press)Google Scholar
  67. 67.
    Masters SL, Latz E, O'Neill LA (2011) The inflammasome in atherosclerosis and type 2 diabetes. Sci Transl Med 3 (in press)Google Scholar
  68. 68.
    Meigs JB, Larson MG, Fox CS, Keaney JF Jr, Vasan RS, Benjamin EJ (2007) Association of oxidative stress, insulin resistance, and diabetes risk phenotypes: the Framingham offspring study. Diabetes Care 30:2529–2535PubMedGoogle Scholar
  69. 69.
    Milagro FI, Campión J, Cordero P, Goyenechea E, Gómez-Uriz AM, Abete I, Zulet MA, Martínez JA (2011) A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J 25:1378–1389PubMedGoogle Scholar
  70. 70.
    Mitra AK, Clarke K (2009) Viral obesity: fact or fiction? Obes Rev 11:289–296PubMedGoogle Scholar
  71. 71.
    Moreno-Aliaga MJ, Campion J, Milagro FI, Berjón A, Martínez JA (2005) Adiposity and proinflammatory state: the chicken or the egg. Adipocytes 1:1–16Google Scholar
  72. 72.
    Nunn AV, Bell JD, Guy GW (2009) Lifestyle-induced metabolic inflexibility and accelerated ageing syndrome: insulin resistance, friend or foe? Nutr Metab (Lond) 6:16. doi:10.1186/1743-7075-6-16
  73. 73.
    O'Hara AM, O'Regan P, Fanning A, O'Mahony C, Macsharry J, Lyons A, Bienenstock J, O'Mahony L, Shanahan F (2006) Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 118:202–215PubMedGoogle Scholar
  74. 74.
    O’Rourke RW, White AE, Metcalf MD, Olivas AS, Mitra P, Larison WG, Cheang EC, Varlamov O, Corless CL, Roberts CT Jr, Marks DL (2011) Hypoxia-induced inflammatory cytokine secretion in human adipose tissue stromovascular cells. Diabetologia 54:1480–1490PubMedGoogle Scholar
  75. 75.
    Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Red Eagle A, Vats D, Brombacher F, Ferrante AW, Chawla A (2007) Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447:1116–1120PubMedGoogle Scholar
  76. 76.
    Ouchi N, Parker JL, Lugus JJ, Walsh K (2011) Adipokines in inflammation and metabolic disease. Nat Rev Immunol 11:85–97PubMedGoogle Scholar
  77. 77.
    Pasarica M, Shin CW, Yu M, Rathod M, Jen KL, MohanKumar S, MohanKumar PS, Markward N, Dhurandhar NV (2006) Human adenovirus 36 induces adiposity, increases insulin sensitivity, and alters hypothalamic monoamines in rats. Obesity 14:1905–1913PubMedGoogle Scholar
  78. 78.
    Perticone F, Ceravolo R, Candigliota M, Ventura G, Iacopino S, Sinopoli F, Mattioli PL (2001) Obesity and body fat distribution induce endothelial dysfunction by oxidative stress: protective effect of vitamin C. Diabetes 50:159–165PubMedGoogle Scholar
  79. 79.
    Poitou C, Lacorte JM, Coupaye M, Bertrais S, Bedel JF, Lafon N, Bouillot JL, Galan P, Borson-Chazot F, Basdevant A, Coussieu C, Clément K (2005) Relationship between single nucleotide polymorphisms in leptin, IL6 andadiponectin genes and their circulating product in morbidly obese subjects before and after gastric banding surgery. Obes Surg 15:11–23PubMedGoogle Scholar
  80. 80.
    Poulain-Godefroy O, Lecoeur C, Pattou F, Frühbeck G, Froguel P (2008) Inflammation is associated with a decrease of lipogenic factors in omental fat in women. Am J Physiol Regul Integr Comp Physiol 295:R1–R7PubMedGoogle Scholar
  81. 81.
    Qatanani M, Lazar MA (2007) Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev 21:1443–1455PubMedGoogle Scholar
  82. 82.
    Ramachandrappa S, Farooqi IS (2011) Genetic approaches to understanding human obesity. J Clin Invest 121:2080–2086PubMedGoogle Scholar
  83. 83.
    Rausch ME, Weisberg S, Vardhana P, Tortoriello DV (2008) Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obes (Lond) 32:451–463Google Scholar
  84. 84.
    Razquin C, Martinez JA, Martinez-Gonzalez MA, Fernandez-Crehuet J, Santos JM, Martinez A (2010) A Mediterranean diet rich in virgin olive oil may reverse the effects of the-174G/C il6 gene variant on 3-year body weight change. Mol Nutr Food Res 54:S75–S82PubMedGoogle Scholar
  85. 85.
    Ricquier D, Bouillaud F (2000) Mitochondrial uncoupling proteins: from mitochondria to the regulation of energy balance. J Physiol 529(Pt 1):3–10PubMedGoogle Scholar
  86. 86.
    Rieusset J, Bouzakri K, Chevillotte E, Ricard N, Jacquet D, Bastard JP, Laville M, Vidal H (2004) Suppressor of cytokine signaling 3 expression and insulin resistance in skeletal muscle of obese and type 2 diabetic patients. Diabetes 53:2232–2241PubMedGoogle Scholar
  87. 87.
    Roberts CK, Sindhu KK (2009) Oxidative stress and metabolic syndrome. Life Sci 84:705–712PubMedGoogle Scholar
  88. 88.
    Rodriguez AM, Palou A (2004) Uncoupling proteins: gender dependence and their relation to body weight control. Int J Obes Relat Metab Disord 28:500–502PubMedGoogle Scholar
  89. 89.
    Rogge MM (2009) The role of impaired mitochondrial lipid oxidation in obesity. Biol Res Nurs 10:356–373PubMedGoogle Scholar
  90. 90.
    Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529PubMedGoogle Scholar
  91. 91.
    Rull A, Camps J, Alonso-Villaverde C, Joven J (2010) Insulin resistance, inflammation, and obesity: role of monocyte chemoattractant protein-1 (or CCL2) in the regulation of metabolism. Mediators Inflamm (in press)Google Scholar
  92. 92.
    Senapedis WT, Kennedy CJ, Boyle PM, Silver PA (2011) Whole genome siRNA cell-based screen links mitochondria to Akt signaling network through uncoupling of electron transport chain. Mol Biol Cell 22:1791–1805PubMedGoogle Scholar
  93. 93.
    Serhan CN, Yang R, Martinod K, Kasuga K, Pillai PS, Porter TF, Oh SF, Spite M (2009) Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. J Exp Med 15:15–23Google Scholar
  94. 94.
    Shaw PJ, Lukens JR, Burns S, Chi H, Mcgargill MA, Kanneganti TD (2010) Cutting edge: critical role for PYCARD/ASC in the development of experimental autoimmune encephalomyelitis. J Immunol 184:4610–4614PubMedGoogle Scholar
  95. 95.
    Silver AE, Beske SD, Christou DD, Donato AJ, Moreau KL, Eskurza I, Gates PE, Seals DR (2007) Overweight and obese humans demonstrate increased vascular endothelial NAD(P)H oxidase-p47(phox) expression and evidence of endothelial oxidative stress. Circulation 115:627–637PubMedGoogle Scholar
  96. 96.
    Song H, Hur DY, Kim KE, Park H, Kim T, Kim CW, Bang S, Cho DH (2006) IL-2/IL-18 prevent the down-modulation of NKG2D by TGF-beta in NK cells via the c-Jun N-terminal kinase (JNK) pathway. Cell Immunol 242:39–45PubMedGoogle Scholar
  97. 97.
    Speliotes EK, Willer CJ, Berndt SI et al (2010) Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nat Genet 42:937–948PubMedGoogle Scholar
  98. 98.
    Stark R, Roden M (2007) Mitochondrial function and endocrine diseases. Eur J Clin Invest 37:236–248PubMedGoogle Scholar
  99. 99.
    Stienstra R, Joosten LA, Koenen T, Van Tits B, Van Diepen JA, Van Den Berg SA, Rensen PC, Voshol PJ, Fantuzzi G, Hijmans A, Kersten S, Muller M, Van Den Berg WB, Van Rooijen N, Wabitsch M, Kullberg BJ, Van Der Meer JW, Kanneganti T, Tack CJ, Netea MG (2010) The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab 12:593–605PubMedGoogle Scholar
  100. 100.
    Sundar Rajan S, Srinivasan V, Balasubramanyam M, Tatu U (2007) Endoplasmic reticulum (ER) stress and diabetes. Indian J Med Res 125:411–424PubMedGoogle Scholar
  101. 101.
    Trayhurn P (2007) Adipocyte biology. Obes Rev 8:41–44PubMedGoogle Scholar
  102. 102.
    Trayhurn P, Wang B, Wood IS (2008) Hypoxia and the endocrine and signalling role of white adipose tissue. Arch Physiol Biochem 114:267–276PubMedGoogle Scholar
  103. 103.
    Valdecantos MP, Pérez-Matute P, Martínez JA (2009) Obesity and oxidative stress: role of antioxidant supplementation. Rev Invest Clin 61:127–139PubMedGoogle Scholar
  104. 104.
    Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD (2011) The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 17:179–188PubMedGoogle Scholar
  105. 105.
    Vangipuram SD, Yu M, Tian J, Stanhope KL, Pasarica M, Havel PJ, Heydari AR, Dhurandhar NV (2007) Adipogenic human adenovirus-36 reduces leptin expression and secretion and increases glucose uptake by fat cells. Int J Obes (Lond) 31:87–96Google Scholar
  106. 106.
    Vitseva OI, Tanriverdi K, Tchkonia TT, Kirkland JL, McDonnell ME, Apovian CM, Freedman J, Gokce N (2008) Inducible Toll-like receptor and NF-kappaB regulatory pathway expression in human adipose tissue. Obesity (Silver Spring) 16:932–937Google Scholar
  107. 107.
    Wang JG, Williams JC, Davis BK, Jacobson K, Doerschuk CM, TingJPY MN (2011) Monocytic microparticles activate endothelialcells in an IL-b-dependent manner. Blood 118:2366–2374PubMedGoogle Scholar
  108. 108.
    Wang B, Wood IS, Trayhurn P (2008) PCR arrays identify metallothionein-3 as a highly hypoxia-inducible gene in human adipocytes. Biochem Biophys Res Commun 368:88–93PubMedGoogle Scholar
  109. 109.
    Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115:1111–1119PubMedGoogle Scholar
  110. 110.
    Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, Brickey WJ, Ting JP (2011) Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 12:408–415PubMedGoogle Scholar
  111. 111.
    Wisse BE, Kim F, Schwartz MW (2007) Physiology. An integrative view of obesity. Science 318:928–929PubMedGoogle Scholar
  112. 112.
    Wood IS, Wang B, Lorente-Cebrian S, Trayhurn P (2007) Hypoxia increases expression of selective facilitative glucose transporters (GLUT) and 2-deoxy-d-glucose uptake in human adipocytes. Biochem Biophys Res Commun 361:468–473PubMedGoogle Scholar
  113. 113.
    Yudkin JS, Coppack SW, Bulmer K, Rawesh A, Mohamed-Ali V (1999) Lack of evidence for secretion of plasminogen activator inhibitor-1 by human subcutaneous adipose tissue in vivo. Thromb Res 96:1–9PubMedGoogle Scholar
  114. 114.
    Zaki MH, Lamkanfi M, Kanneganti TD (2011) The Nlrp3 inflammasome: contributions to intestinal homeostasis. Trends Immunol 32:171–179PubMedGoogle Scholar
  115. 115.
    Zeyda M, Stulnig TM (2009) Obesity, inflammation, and insulin resistance—a mini-review. Gerontology 55:379–86PubMedGoogle Scholar
  116. 116.
    Zhao Y, He X, Shi X, Huang C, Liu J, Zhou S, Heng CK (2010) Association between serum amyloid A and obesity: a meta-analysis and systematic review. Inflamm Res 59:323–334PubMedGoogle Scholar

Copyright information

© University of Navarra 2012

Authors and Affiliations

  • Isabel Bondia-Pons
    • 1
  • Lisa Ryan
    • 2
  • J. Alfredo Martinez
    • 1
  1. 1.Department of Nutrition, Food Science, Physiology and Toxicology Research BuildingUniversity of NavarraPamplonaSpain
  2. 2.Functional Food Centre, Department of Sport and Health SciencesOxford Brookes UniversityOxfordUK

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