Periodontitis as a novel contributor of adipose tissue inflammation promotes insulin resistance in a rat model

Journal of Periodontology

Volumn 84, Issue 11, 2013, Pages 1617-1626

  Su, Yuan ^a   Wang, Dan ^a   Xuan, Dongying ^a   Ni, Jia ^a   Luo, Shigao ^a   Xie, Baoyi ^a   Zhang, Jincai ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Adipose tissue; Inflammation; Insulin resistance; Macrophages; Pancreas; Periodontitis.

Indexed keywords

CD14 ANTIGEN; CD68 PROTEIN, RAT; DIFFERENTIATION ANTIGEN; FLAVORING AGENT; GLUTAMATE SODIUM; INSULIN; LEUKOCYTE ANTIGEN;

ADIPOCYTE; ALVEOLAR BONE LOSS; ANIMAL; ARTICLE; BLOOD; CELL COUNT; CELL SHAPE; COMPARATIVE STUDY; DIET RESTRICTION; DISEASE MODEL; GLUCOSE BLOOD LEVEL; INSULIN RESISTANCE; MACROPHAGE; MALE; METHODOLOGY; MICRO-COMPUTED TOMOGRAPHY; OBESITY; PATHOLOGY; PERIODONTITIS; PHENOTYPE; PHYSIOLOGY; RANDOMIZATION; RAT; SPRAGUE DAWLEY RAT; STROMA CELL; THREE DIMENSIONAL IMAGING; TIME; WHITE ADIPOSE TISSUE;

ADIPOCYTES; ADIPOSE TISSUE, WHITE; ALVEOLAR BONE LOSS; ANIMALS; ANTIGENS, CD; ANTIGENS, CD14; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BLOOD GLUCOSE; CELL COUNT; CELL SHAPE; DISEASE MODELS, ANIMAL; FASTING; FLAVORING AGENTS; IMAGING, THREE-DIMENSIONAL; INSULIN; INSULIN RESISTANCE; MACROPHAGES; MALE; OBESITY; PERIODONTITIS; PHENOTYPE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SODIUM GLUTAMATE; STROMAL CELLS; TIME FACTORS; X-RAY MICROTOMOGRAPHY;

EID: 84888333455     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2013.120442     Document Type: Article

References (43)

1. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest 2005;115:1111-1119.
2. Scherer PE. Adipose tissue: From lipid storage compartment to endocrine organ. Diabetes 2006;55:1537-1545.
3. Satoh M, Andoh Y, Clingan CS, et al. Type II NKT cells stimulate diet-induced obesity by mediating adipose tissue inflammation, steatohepatitis and insulin resistance. PLoS ONE 2012;7:e30568.
4. Khan RS, Kato TS, Chokshi A, et al. Adipose tissue inflammation and adiponectin resistance in patients with advanced heart failure: Correction after ventricular assist device implantation. Circ Heart Fail 2012;5: 340-348.
5. Huo Y, Guo X, Li H, et al. Disruption of inducible 6-phosphofructo-2- kinase ameliorates diet-induced adiposity but exacerbates systemic insulin resistance and adipose tissue inflammatory response. J Biol Chem 2010;285:3713-3721.
6. Dyck DJ, Heigenhauser GJ, Bruce CR. The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol (Oxf) 2006;186:5-16.
7. Balistreri CR, Caruso C, Candore G. The role of adipose tissue and adipokines in obesity-related inflammatory diseases. Mediators Inflamm 2010; 2010:802078.
8. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005;366:1809-1820.
9. Saito T, Shimazaki Y, Sakamoto M. Obesity and periodontitis. N Engl J Med 1998;339:482-483.
10. Saxlin T, Ylostalo P, Suominen-Taipale L, Mannisto S, Knuuttila M. Association between periodontal infection and obesity: Results of the Health 2000 Survey. J Clin Periodontol 2011;38:236-242.
11. Morita I, Okamoto Y, Yoshii S, et al. Five-year incidence of periodontal disease is related to body mass index. J Dent Res 2011;90:199-202.
12. Lalla E, Papapanou PN. Diabetes mellitus and periodontitis: A tale of two common interrelated diseases. Nat Rev Endocrinol 2011;7:738-748.
13. Gorman A, Kaye EK, Nunn M, Garcia RI. Changes in body weight and adiposity predict periodontitis progression in men. J Dent Res 2012;91:921-926.
14. Pischon N, Heng N, Bernimoulin JP, Kleber BM, Willich SN, Pischon T. Obesity, inflammation, and periodontal disease. J Dent Res 2007;86:400-409.
15. Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: A two-way relationship. Diabetologia 2012; 55:21-31.
16. Watanabe K, Petro BJ, Shlimon AE, Unterman TG. Effect of periodontitis on insulin resistance and the onset of type 2 diabetes mellitus in Zucker diabetic fatty rats. J Periodontol 2008;79:1208-1216.
17. Ekuni D, Tomofuji T, Irie K, et al. Effects of periodontitis on aortic insulin resistance in an obese rat model. Lab Invest 2010;90:348-359.
18. Endo Y, Tomofuji T, Ekuni D, et al. Experimental periodontitis induces gene expression of proinflammatory cytokines in liver and white adipose tissues in obesity. J Periodontol 2010;81:520-526.
19. Macho L, Ficková M, Jezová, Zó rad S. Late effects of postnatal administration of monosodium glutamate on insulin action in adult rats. Physiol Res 2000;49 (Suppl. 1):S79-S85.
20. Nagata M, Suzuki W, Iizuka S, et al. Type 2 diabetes mellitus in obese mouse model induced by monosodium glutamate. Exp Anim 2006;55:109-115.
21. Park CH, Abramson ZR, Taba MJ JrJr., et al. Threedimensional micro-computed tomographic imaging of alveolar bone in experimental bone loss or repair. J Periodontol 2007;78:273-281.
22. Li P, Lu M, Nguyen MT, et al. Functional heterogeneity of CD11c-positive adipose tissue macrophages in dietinduced obese mice. J Biol Chem 2010;285:15333-15345.
23. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412-419.
24. Pejcic A, Kesic LJ, Milasin J. C-reactive protein as a systemic marker of inflammation in periodontitis. Eur J Clin Microbiol Infect Dis 2011;30:407-414.
25. Haba D, Teslaru S, Ungureanu D, et al. Evaluation of serum and gingival crevicular fluid C-reactive protein and IL-6 levels in patients with periodontitis and transient ischemic attacks. Rom J Morphol Embryol 2011;52:1243-1247.
26. D'Aiuto F, Parkar M, Andreou G, et al. Periodontitis and systemic inflammation: Control of the local infection is associated with a reduction in serum inflammatory markers. J Dent Res 2004;83:156-160.
27. Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, De Nardin E. Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol 2001;72:1221-1227.
28. Marcaccini AM, Meschiari CA, Sorgi CA, et al. Circulating interleukin-6 and high-sensitivity C-reactive protein decrease after periodontal therapy in otherwise healthy subjects. J Periodontol 2009;80:594-602.
29. Chen L, Luo G, Xuan D, et al. Effects of non-surgical periodontal treatment on clinical response, serum inflammatory parameters, and metabolic control in patients with type 2 diabetes: A randomized study. J Periodontol 2012;83:435-443.
30. Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL, Newman HN, Battino M. Metabolic syndrome and periodontitis: Is oxidative stress a common link? J Dent Res 2009;88:503-518.
31. Mohamed-Ali V, Goodrick S, Rawesh A, et al. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-Alpha, in vivo. J Clin Endocrinol Metab 1997;82:4196-4200.
32. Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays a crucial role in the development of obesityrelated insulin resistance. J Clin Invest 2003;112: 1821-1830.
33. Zimmermann GS, Bastos MF, Dias GT, Chambrone L, Duarte PM. Local and circulating levels of adipocytokines in obese and normal weight individuals with chronic periodontitis. J Periodontol 2012;83:27-35.
34. Maury E, Brichard SM. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 2010;314:1-16.
35. Spalding KL, Arner E, Westermark PO, et al. Dynamics of fat cell turnover in humans. Nature 2008;453:783-787.
36. Jernas M, Palming J, Sjoholm K, et al. Separation of human adipocytes by size: Hypertrophic fat cells display distinct gene expression. FASEB J 2006;20: 1540-1542.
37. Skurk T, Alberti-Huber C, Herder C, Hauner H. Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 2007; 92:1023-1033.
38. Fain JN, Bahouth SW, Madan AK. TNFalpha release by the nonfat cells of human adipose tissue. Int J Obes Relat Metab Disord 2004;28:616-622.
39. Maury E, Noel L, Detry R, Brichard SM. In vitro hyperresponsiveness to tumor necrosis factor-Alpha contributes to adipokine dysregulation in omental adipocytes of obese subjects. J Clin Endocrinol Metab 2009;94:1393-1400.
40. Ohashi K, Parker JL, Ouchi N, et al. Adiponectin promotes macrophage polarization toward an antiinflammatory phenotype. J Biol Chem 2010;285: 6153-6160.
41. Fernández-Real JM, Pérez del Pulgar S, Luche E, et al. CD14 modulates inflammation-driven insulin resistance. Diabetes 2011;60:2179-2186.
42. Allen EM, Matthews JB, O'Halloran DJ, Griffiths HR, Chapple IL. Oxidative and inflammatory status in type 2 diabetes patients with periodontitis. J Clin Periodontol 2011;38:894-901.
43. Colombo NH, Shirakashi DJ, Chiba FY, et al. Periodontal disease decreases insulin sensitivity and insulin signaling. J Periodontol 2012;83:864-870.