Differential Impact of Weight Loss and Glycemic Control on Inflammasome Signaling.
Journal
Obesity (Silver Spring, Md.)
ISSN: 1930-739X
Titre abrégé: Obesity (Silver Spring)
Pays: United States
ID NLM: 101264860
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
16
07
2019
accepted:
03
12
2019
pubmed:
6
2
2020
medline:
2
9
2020
entrez:
6
2
2020
Statut:
ppublish
Résumé
Interleukin (IL)-1β is involved in obesity-associated inflammation and in the pathogenesis of type 2 diabetes (T2D) mellitus. Our aim was to correlate serum IL-1β and caspase-1 levels with weight loss, glucose metabolism, and insulin resistance (IR) after bariatric surgery. A total of 32 patients with morbid obesity and T2D (Ob-T2D) and 29 patients with morbid obesity and normal glucose tolerance (Ob-NGT), treated by Roux-en-Y gastric bypass, were studied before and 1 year after surgery. Sixteen healthy individuals served as a control (HC) group. IR was assessed by the oral glucose insulin sensitivity method. Plasma IL-1β levels and caspase-1 were measured. Presurgery BMI was similar in Ob-NGT and Ob-T2D. IR was progressively impaired in Ob-NGT and Ob-T2D (P < 0.0001). Fasting plasma IL-1β and caspase-1 levels were lower in HCs than in patients with Ob-NGT or Ob-T2D (P < 0.02; P = 0.05), and both were inversely correlated with IR (P = 0.01; P = 0.02). After surgery, BMI decreased and IR improved to a similar extent in Ob-NGT and Ob-T2D (P < 0.0001). Plasma caspase-1 concentrations normalized in both groups (P < 0.0001), whereas plasma IL-1β levels normalized only in Ob-NGT. Plasma IL-1β and caspase-1 levels were inversely correlated with IR. Caspase-1 levels normalized after weight loss, whereas IL-1β normalized only in people without T2D, suggesting the persistence of a systemic inflammatory condition in people with T2D.
Substances chimiques
Blood Glucose
0
IL1B protein, human
0
Inflammasomes
0
Interleukin-1beta
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
609-615Subventions
Organisme : EMIF grant (IMI JU GA 115372-2).
ID : (IMI JU GA 115372-2).
Pays : International
Informations de copyright
© 2020 The Obesity Society.
Références
Global BMI Mortality Collaboration; Di Angelantonio E, Bhupathiraju ShN, Wormser D, et al. Body-mass index and all-cause mortality: individual-participant-data meta-analysis of 239 prospective studies in four continents. Lancet 2016;388:776-786.
Andersen CJ, Murphy KE, Fernandez ML. Impact of obesity and metabolic syndrome on immunity. Adv Nutr 2016;7:66-75.
Ota T. Obesity-induced inflammation and insulin resistance. Front Endocrinol 2014;5:204. doi:10.3389/fendo.2014.00204
Yudkin JS. Adipose tissue, insulin action and vascular disease: inflammatory signals. Int J Obes Relat Metab Disord 2003;27(suppl 3):S25-S28.
Stienstra R, Tack CJ, Kanneganti TD, Joosten LA, Netea MG. The inflammasome puts obesity in the danger zone. Cell Metab 2012;15:10-18.
Boutens L, Stienstra R. Adipose tissue macrophages: going off track during obesity. Diabetologia 2016;59:879-894.
Chawla A, Nguyen KD, Goh YP. Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol 2011;11:738-749.
Pellegrini C, Antonioli L, Lopez-Castejon G, Blandizzi C, Fornai M. Canonical and non-canonical activation of NLRP3 inflammasome at the crossroad between immune tolerance and intestinal inflammation. Front Immunol 2017;8:36. doi:10.3389/fimmu.2017.00036
Cocco M, Pellegrini C, Martínez-Banaclocha H, et al. Development of an acrylate derivative targeting the NLRP3 inflammasome for the treatment of inflammatory bowel disease. J Med Chem 2017;60:3656-3671.
Csoka B, Toro G, Vindeirinho J, et al. A2A adenosine receptors control pancreatic dysfunction in high-fat-diet-induced obesity. FASEB J 2017;31:4985-4997.
Antonioli L, Blandizzi C, Csóka B, Pacher P, Haskó G. Adenosine signalling in diabetes mellitus-pathophysiology and therapeutic considerations. Nat Rev Endocrinol 2015;11:228-241.
CsókaB, KoscsóB, TöroG, et al. A2B adenosine receptors prevent insulin resistance by inhibiting adipose tissue inflammation via maintaining alternative macrophage activation. Diabetes 2014;63:850-866.
Németh ZH, Bleich D, Csóka B, et al. Adenosine receptor activation ameliorates type 1 diabetes. FASEB J 2007;21:2379-2388.
Lee HM, Kim JJ, Kim HJ, Shong M, Ku BJ, Jo EK. Upregulated NLRP3 inflammasome activation in patients with type 2 diabetes. Diabetes 2013;62:194-204.
Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 2011;11:98-107.
Nannipieri M, Mari A, Anselmino M, et al. The role of beta-cell function and insulin sensitivity in the remission of type 2 diabetes after gastric bypass surgery. J Clin Endocrinol Metab 2011;96:E1372-E1379.
Pournaras DJ, Aasheim ET, Sovik TT, et al. Effect of the definition of type II diabetes remission in the evaluation of bariatric surgery for metabolic disorders. Br J Surg 2012;99:100-103.
Brethauer SA, Aminian A, Romero-Talamás H, et al. Can diabetes be surgically cured? Long-term metabolic effects of bariatric surgery in obese patients with type 2 diabetes mellitus. Ann Surg 2013;258:628-636; discussion 636-627.
Chiappetta S, Schaack HM, Wölnerhannsen B, Stier C, Squillante S, Weiner RA. The impact of obesity and metabolic surgery on chronic inflammation. Obes Surg 2018;28:3028-3040.
Hanusch-Enserer U, Cauza E, Spak M, et al. Acute-phase response and immunological markers in morbid obese patients and patients following adjustable gastric banding. Int J Obes Relat Metab Disord 2003;27:355-361.
van Dielen FM, Buurman WA, Hadfoune M, Nijhuis J, Greve JW. Macrophage inhibitory factor, plasminogen activator inhibitor-1, other acute phase proteins, and inflammatory mediators normalize as a result of weight loss in morbidly obese subjects treated with gastric restrictive surgery. J Clin Endocrinol Metab 2004;89:4062-4068.
Santos J, Salgado P, Santos C, et al. Effect of bariatric surgery on weight loss, inflammation, iron metabolism, and lipid profile. Scand J Surg 2014;103:21-25.
Rao SR. Inflammatory markers and bariatric surgery: a meta-analysis. Inflamm Res 2012;61:789-807.
American Diabetes Association. 2. Classification and diagnosis of diabetes: Standards of Medical Care in Diabetes-2019. Diabetes Care 2019;42(suppl 1):S13-S28.
Robertson S, Martínez GJ, Payet CA, et al. Colchicine therapy in acute coronary syndrome patients acts on caspase-1 to suppress NLRP3 inflammasome monocyte activation. Clin Sci 2016;130:1237-1246.
Blankenberg S, Godefroy T, Poirier O, et al. Haplotypes of the caspase-1 gene, plasma caspase-1 levels, and cardiovascular risk. Circ Res 2006;99:102-108.
Fortuño A, Rodríguez A, Gómez-Ambrosi J, Frühbeck G, Díez J. Adipose tissue as an endocrine organ: role of leptin and adiponectin in the pathogenesis of cardiovascular diseases. J Physiol Biochem 2003;59:51-60.
Khaodhiar L, Ling PR, Blackburn GL, Bistrian BR. Serum levels of interleukin-6 and C-reactive protein correlate with body mass index across the broad range of obesity. JPEN J Parenter Enteral Nutr 2004;28:410-415.
Hotamisligil GS. Inflammatory pathways and insulin action. Int J Obes Relat Metab Disord 2003;27(suppl 3):S53-S55.
Maedler K, Sergeev P, Ris F, et al. Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets. J Clin Investig 2017;127:1589. doi:10.1172/JCI92172
Moschen AR, Molnar C, Enrich B, Geiger S, Ebenbichler CF, Tilg H. Adipose and liver expression of interleukin (IL)-1 family members in morbid obesity and effects of weight loss. Mol Med 2011;17:840-845.
Strowig T, Henao-Mejia J, Elinav E, Flavell R. Inflammasomes in health and disease. Nature 2012;481:278-286.
Leemans JC, Cassel SL, Sutterwala FS. Sensing damage by the NLRP3 inflammasome. Immunol Rev 2011;243:152-162.
Rheinheimer J, de Souza BM, Cardoso NS, Bauer AC, Crispim D. Current role of the NLRP3 inflammasome on obesity and insulin resistance: a systematic review. Metabolism 2017;74:1-9.
Verheggen R, Eijsvogels TMH, Catoire M, et al. Cytokine responses to repeated, prolonged walking in lean versus overweight/obese individuals. J Sci Med Sport 2019;22:196-200.
Pahwa R, Adams-Huet B, Jialal I. The effect of increasing body mass index on cardio-metabolic risk and biomarkers of oxidative stress and inflammation in nascent metabolic syndrome. J Diabetes Complications 2017;31:810-813.
Jung C, Gerdes N, Fritzenwanger M, Figulla HR. Circulating levels of interleukin-1 family cytokines in overweight adolescents. Mediators Inflamm 2010;2010:958403. doi:10.1155/2010/958403
Spranger J, Kroke A, Mohlig M, et al. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 2003;52:812-817.
Ruscitti P, Cipriani P, Di Benedetto P, et al. Monocytes from patients with rheumatoid arthritis and type 2 diabetes mellitus display an increased production of interleukin (IL)-1beta via the nucleotide-binding domain and leucine-rich repeat containing family pyrin 3(NLRP3)-inflammasome activation: a possible implication for therapeutic decision in these patients. Clin Exp Immunol 2015;182:35-44.
Dalmas E, Venteclef N, Caer C, et al. T cell-derived IL-22 amplifies IL-1beta-driven inflammation in human adipose tissue: relevance to obesity and type 2 diabetes. Diabetes 2014;63:1966-1977.
Nosso G, Lupoli R, Saldalamacchia G, et al. Diabetes remission after bariatric surgery is characterized by high glycemic variability and high oxidative stress. Nutr Metab Cardiovasc Dis 2017;27:949-955.
Monnier L, Mas E, Ginet C, et al. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA 2006;295:1681-1687.
Chang CM, Hsieh CJ, Huang JC, Huang IC. Acute and chronic fluctuations in blood glucose levels can increase oxidative stress in type 2 diabetes mellitus. Acta Diabetol 2012;49(suppl 1):S171-S177.
Vandanmagsar B, Youm YH, Ravussin A, et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 2011;17:179-188.
Goossens GH, Blaak EE, Theunissen R, et al. Expression of NLRP3 inflammasome and T cell population markers in adipose tissue are associated with insulin resistance and impaired glucose metabolism in humans. Mol Immunol 2012;50:142-149.